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The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1991 Aug 1;174(2):397–406. doi: 10.1084/jem.174.2.397

Early separation of B and T lymphocyte precursors in chick embryo

PMCID: PMC2118911  PMID: 1856628

Abstract

Embryonic chimeras were used to demonstrate an early separation of chicken T and B cell precursors. Genetically polymorphic cell surface antigens, Bu-1 and Ov, which are expressed on cells of the B and T lineage, respectively, are useful markers in adoptive cell transfer studies. Allelic products Bu-1a and Bu-1b can be detected with monoclonal antibodies (mAbs) L22 and 11G2, respectively, and the Ov antigen with mAb 11A9. Chimeric chickens were constructed by reconstituting irradiated 14-d Ov- H.B19 embryos with the sorted Bu-1+ or Bu-1- fractions of spleen cells from age-matched H.B19 Ov+ embryos. Chimeras were analyzed, 3-4 wk after hatching, for the presence of Ov+ cells in the bursa, thymus, spleen, and peripheral blood lymphocytes. T cell precursors giving rise to thymocytes and peripheral T cells were present only in the Bu-1-, but not in the Bu-1+, fraction. We previously demonstrated that, in contrast, all B cell precursors in spleen from 14-d embryos are exclusively present in the Bu-1+ fraction. We also analyzed the immunoglobulin light chain gene rearrangement in these populations by polymerase chain reaction. We show here that VJ recombination occurs in the Bu-1+, but not in the Bu-1-, fraction of spleen. These data demonstrate an early commitment to the B cell lineage, which occurs before the colonization of the bursa of Fabricius. Segregation of B cell precursors from the other hemopoietic precursors, and consequently separation of T and B cell precursors, occurs before the colonization of the primary lymphoid organs.

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Selected References

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  1. Chen C. L., Bucy R. P., Cooper M. D. T cell differentiation in birds. Semin Immunol. 1990 Jan;2(1):79–86. [PubMed] [Google Scholar]
  2. Cooper M. D., Raymond D. A., Peterson R. D., South M. A., Good R. A. The functions of the thymus system and the bursa system in the chicken. J Exp Med. 1966 Jan 1;123(1):75–102. doi: 10.1084/jem.123.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Houssaint E. Cell lineage segregation during bursa of Fabricius ontogeny. J Immunol. 1987 Jun 1;138(11):3626–3634. [PubMed] [Google Scholar]
  4. Houssaint E., Diez E., Pink J. R. Ontogeny and tissue distribution of the chicken Bu-1a antigen. Immunology. 1987 Nov;62(3):463–470. [PMC free article] [PubMed] [Google Scholar]
  5. Houssaint E., Lassila O., Vainio O. Bu-1 antigen expression as a marker for B cell precursors in chicken embryos. Eur J Immunol. 1989 Feb;19(2):239–243. doi: 10.1002/eji.1830190204. [DOI] [PubMed] [Google Scholar]
  6. Houssaint E., Tobin S., Cihak J., Lösch U. A chicken leukocyte common antigen: biochemical characterization and ontogenetic study. Eur J Immunol. 1987 Feb;17(2):287–290. doi: 10.1002/eji.1830170221. [DOI] [PubMed] [Google Scholar]
  7. Houssaint E., Toraño A., Ivanyi J. Ontogenic restriction of colonization of the bursa of Fabricius. Eur J Immunol. 1983 Jul;13(7):590–595. doi: 10.1002/eji.1830130715. [DOI] [PubMed] [Google Scholar]
  8. Jalkanen S., Granfors K., Jalkanen M., Toivanen P. Immune capacity of the chicken bursectomized at 60 hr of incubation: surface immunoglobulin and B-L (La-like) antigen-bearing cells. J Immunol. 1983 May;130(5):2038–2041. [PubMed] [Google Scholar]
  9. Jotereau F. V., Le Douarin N. M. Demonstration of a cyclic renewal of the lymphocyte precursor cells in the quail thymus during embryonic and perinatal life. J Immunol. 1982 Nov;129(5):1869–1877. [PubMed] [Google Scholar]
  10. Kaufman J. F., Flajnik M. F., Du Pasquier L., Riegert P. Xenopus MHC class II molecules. I. Identification and structural characterization. J Immunol. 1985 May;134(5):3248–3257. [PubMed] [Google Scholar]
  11. Lassila O., Alanen A., Vainio O., Houssaint E., Pink J. R., Weber W. T. B cell precursors in chick embryos surgically bursectomized at 72 h of incubation. Eur J Immunol. 1988 Nov;18(11):1867–1870. doi: 10.1002/eji.1830181136. [DOI] [PubMed] [Google Scholar]
  12. Le Douarin N. M., Jotereau F. V. Tracing of cells of the avian thymus through embryonic life in interspecific chimeras. J Exp Med. 1975 Jul 1;142(1):17–40. doi: 10.1084/jem.142.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mansikka A., Jalkanen S., Sandberg M., Granfors K., Lassila O., Toivanen P. Bursectomy of chicken embryos at 60 hours of incubation leads to an oligoclonal B cell compartment and restricted Ig diversity. J Immunol. 1990 Dec 1;145(11):3601–3609. [PubMed] [Google Scholar]
  14. Mansikka A., Sandberg M., Lassila O., Toivanen P. Rearrangement of immunoglobulin light chain genes in the chicken occurs prior to colonization of the embryonic bursa of Fabricius. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9416–9420. doi: 10.1073/pnas.87.23.9416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Moore M. A., Owen J. J. Experimental studies on the development of the bursa of Fabricius. Dev Biol. 1966 Aug;14(1):40–51. doi: 10.1016/0012-1606(66)90004-2. [DOI] [PubMed] [Google Scholar]
  16. Pink J. R., Rijnbeek A. M. Monoclonal antibodies against chicken lymphocyte surface antigens. Hybridoma. 1983;2(3):287–296. doi: 10.1089/hyb.1983.2.287. [DOI] [PubMed] [Google Scholar]
  17. Ratcliffe M. J. Generation of immunoglobulin heavy chain diversity subsequent to cell surface immunoglobulin expression in the avian bursa of Fabricius. J Exp Med. 1989 Oct 1;170(4):1165–1173. doi: 10.1084/jem.170.4.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Reynaud C. A., Anquez V., Dahan A., Weill J. C. A single rearrangement event generates most of the chicken immunoglobulin light chain diversity. Cell. 1985 Feb;40(2):283–291. doi: 10.1016/0092-8674(85)90142-4. [DOI] [PubMed] [Google Scholar]
  19. Reynaud C. A., Anquez V., Grimal H., Weill J. C. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell. 1987 Feb 13;48(3):379–388. doi: 10.1016/0092-8674(87)90189-9. [DOI] [PubMed] [Google Scholar]
  20. Reynaud C. A., Dahan A., Anquez V., Weill J. C. Somatic hyperconversion diversifies the single Vh gene of the chicken with a high incidence in the D region. Cell. 1989 Oct 6;59(1):171–183. doi: 10.1016/0092-8674(89)90879-9. [DOI] [PubMed] [Google Scholar]
  21. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  22. Thompson C. B., Neiman P. E. Somatic diversification of the chicken immunoglobulin light chain gene is limited to the rearranged variable gene segment. Cell. 1987 Feb 13;48(3):369–378. doi: 10.1016/0092-8674(87)90188-7. [DOI] [PubMed] [Google Scholar]
  23. Toivanen P., Toivanen A. Bursal and postbursal stem cells in chicken. Functional characteristics. Eur J Immunol. 1973 Sep;3(9):585–595. doi: 10.1002/eji.1830030912. [DOI] [PubMed] [Google Scholar]
  24. Vainio O., Lassila O., Cihak J., Lösch U., Houssaint E. Tissue distribution and appearance in ontogeny of alpha/beta T cell receptor (TCR2) in chicken. Cell Immunol. 1990 Jan;125(1):254–260. doi: 10.1016/0008-8749(90)90079-7. [DOI] [PubMed] [Google Scholar]
  25. WARNER N. L., SZENBERG A., BURNET F. M. The immunological role of different lymphoid organs in the chicken. I. Dissociation of immunological responsiveness. Aust J Exp Biol Med Sci. 1962 Oct;40:373–387. doi: 10.1038/icb.1962.42. [DOI] [PubMed] [Google Scholar]
  26. Weber W. T., Alexander J. E. The potential of bursa-immigrated hematopoietic precursor cells to differentiate to functional B and T cells. J Immunol. 1978 Aug;121(2):653–657. [PubMed] [Google Scholar]
  27. Weber W. T., Mausner R. Migration patterns of avian embryonic bone marrow cells and their differentiation to functional T and B cells. Adv Exp Med Biol. 1977;88:47–59. doi: 10.1007/978-1-4613-4169-7_5. [DOI] [PubMed] [Google Scholar]

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