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. 1979 May;37(1):123–134.

B-cell precursors in early chicken embryos.

A M Lebacq, M A Ritter
PMCID: PMC1457309  PMID: 381171

Abstract

The ontogeny of B-cell precursors in chicken embryos from day 3 of incubation onwards has been studied. Purified antibodies to chicken Ig L, gamma, mu, alpha chains were used in a sensitive indirect immunofluorescence assayed on fixed cell smears and wax-embedded tissue sections; the location and morphology of immunoglobulin positive (Ig+) cells were determined either in phase contrast or after histological staining. Lymphoid cells containing small amounts of cytoplasmic immunoglobulin were found in 3 day and older embryonic yolk sac, 11 and 12 day blood, 11, 12 and 13 day bursal mesenchyme. cIg+ large basophilic cells were first seen in 14 day bursal follicles. It is concluded that cells enter the embryonic bursa at different developmental stages: some appear to be uncommitted stem cells, whilst others have already commenced B-cell maturation in an extra-bursal site.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ACKERMAN G. A., KNOUFF R. A. Lymphocytopoiesis in the bursa of Fabricius. Am J Anat. 1959 Mar;104:163–205. doi: 10.1002/aja.1001040202. [DOI] [PubMed] [Google Scholar]
  2. Albini B., wick G. Ontogeny of lymphoid cell surface determinants in the chicken. Int Arch Allergy Appl Immunol. 1975;48(4):513–529. doi: 10.1159/000231339. [DOI] [PubMed] [Google Scholar]
  3. BURSTEIN M., SAMAILLE J. Nouvelle methode de séparation et de dosage des lipoprotéines de faible densité. Ann Biol Clin (Paris) 1959 Jan-Feb;17(1-2):23–34. [PubMed] [Google Scholar]
  4. Bienenstock J., Perey D. Y., Gauldie J., Underdown B. J. Chicken immunoglobulin resembling A. J Immunol. 1972 Aug;109(2):403–406. [PubMed] [Google Scholar]
  5. CRUMPTON M. J., WILKINSON J. M. AMINO ACID COMPOSITIONS OF HUMAN AND RABBIT GAMMA-GLOBULINS AND OF THE FRAGMENTS PRODUCED BY REDUCTION. Biochem J. 1963 Aug;88:228–234. doi: 10.1042/bj0880228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cambiaso C. L., Goffinet A., Vaerman J. P., Heremans J. F. Glutaraldehyde-activated aminohexyl- derivative of Sepharose 4B as a new verstile immunoabsorbent. Immunochemistry. 1975 Apr;12(4):273–278. doi: 10.1016/0019-2791(75)90175-5. [DOI] [PubMed] [Google Scholar]
  7. Claflin A. J., Smithies O., Meyer R. K. Antibody responses in bursa-deficient chickens. J Immunol. 1966 Nov;97(5):693–699. [PubMed] [Google Scholar]
  8. Dieterlen-Lievre F. On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. J Embryol Exp Morphol. 1975 Jun;33(3):607–619. [PubMed] [Google Scholar]
  9. Du Pasquier L. Ontogeny of the immune response in animals having less than one million lymphocytes: the larvae of the toad Alytes obstetricans. Immunology. 1970 Aug;19(2):353–362. [PMC free article] [PubMed] [Google Scholar]
  10. Fitzsimmons R. C., Garrod E. M., Garnett I. Immunological responses following early embryonic surgical bursectomy. Cell Immunol. 1973 Dec;9(3):377–383. doi: 10.1016/0008-8749(73)90052-x. [DOI] [PubMed] [Google Scholar]
  11. Gathings W. E., Lawton A. R., Cooper M. D. Immunofluorescent studies of the development of pre-B cells, B lymphocytes and immunoglobulin isotype diversity in humans. Eur J Immunol. 1977 Nov;7(11):804–810. doi: 10.1002/eji.1830071112. [DOI] [PubMed] [Google Scholar]
  12. Janković B. D., Isaković K., Marković B. M., Rajcević M., Knezević Z. Nonbursal origin of humoral immunity: immune capacity and cytomorphological changes in chickens bursectomized as 52- to 64-hours-old embryos. Exp Hematol. 1976 Jul;4(4):246–255. [PubMed] [Google Scholar]
  13. Kincade P. W., Cooper M. D. Development and distribution of immunoglobulin-containing cells in the chicken. An immunofluorescent analysis using purified antibodies to mu, gamma and light chains. J Immunol. 1971 Feb;106(2):371–382. [PubMed] [Google Scholar]
  14. Lawton A. R., Kincade P. W., Cooper M. D. Sequential expression of germ line genes in development of immunoglobulin class diversity. Fed Proc. 1975 Jan;34(1):33–39. [PubMed] [Google Scholar]
  15. Le Douarin N. M., Houssaint E., Jotereau F. V., Belo M. Origin of hemopoietic stem cells in embryonic bursa of Fabricius and bone marrow studied through interspecific chimeras. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2701–2705. doi: 10.1073/pnas.72.7.2701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lebacq-Verheyden A. M., Vaerman J. P., Heremans J. F. A possible homologue of mammalian IgA in chicken serum and secretions. Immunology. 1972 Jan;22(1):165–175. [PMC free article] [PubMed] [Google Scholar]
  17. Lebacq-Verheyden A. M., Vaerman J. P., Heremans J. F. Immunohistologic distribution of the chicken immunoglobulins. J Immunol. 1972 Sep;109(3):652–654. [PubMed] [Google Scholar]
  18. Lebacq-Verheyden A. M., Vaerman J. P., Heremans J. F. Quantification and distribution of chicken immunoglobulins IgA, IgM and IgG in serum and secretions. Immunology. 1974 Oct;27(4):683–692. [PMC free article] [PubMed] [Google Scholar]
  19. Lerner K. G., Glick B., McDuffie F. C. Role of the bursa of Fabricius in IgG and IgM production in the chicken: evidence for the role of a non-bursal site in the development of humoral immunity. J Immunol. 1971 Aug;107(2):493–503. [PubMed] [Google Scholar]
  20. Leslie G. A., Clem L. W. Phylogen of immunoglobulin structure and function. 3. Immunoglobulins of the chicken. J Exp Med. 1969 Dec 1;130(6):1337–1352. doi: 10.1084/jem.130.6.1337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lydyard P. M., Grossi C. E., Cooper M. D. Ontogeny of B cells in the chicken. I. Sequential development of clonal diversity in the bursa. J Exp Med. 1976 Jul 1;144(1):79–97. doi: 10.1084/jem.144.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Martin L. N., Leslie G. A. IgM-forming cells as the immediate precursor of IgA-producing cells during ontogeny of the immunoglobulin-producing system of the chicken. J Immunol. 1974 Jul;113(1):120–126. [PubMed] [Google Scholar]
  23. Melchers F., Von Boehmer H., Phillips R. A. B-lymphocyte subpopulations in the mouse. Organ distribution and ontogeny of immunoglobulin-synthesizing and of mitogen-sensitive cells. Transplant Rev. 1975;25:26–58. doi: 10.1111/j.1600-065x.1975.tb00725.x. [DOI] [PubMed] [Google Scholar]
  24. Nossal G. J., Pike B. L. Differentiation of B lymphocytes from stem cell precursors. Adv Exp Med Biol. 1973;29(0):11–18. doi: 10.1007/978-1-4615-9017-0_3. [DOI] [PubMed] [Google Scholar]
  25. Owen J. J., Cooper M. D., Raff M. C. In vitro generation of B lymphocytes in mouse foetal liver, a mammalian 'bursa equivalent'. Nature. 1974 May 24;249(455):361–363. doi: 10.1038/249361a0. [DOI] [PubMed] [Google Scholar]
  26. Ploem J. S. The use of a vertical illuminator with interchangeable dichroic mirrors for fluorescence microscopy with incidental light. Z Wiss Mikrosk. 1967 Nov;68(3):129–142. [PubMed] [Google Scholar]
  27. Raff M. C., Megson M., Owen J. J., Cooper M. D. Early production of intracellular IgM by B-lymphocyte precursors in mouse. Nature. 1976 Jan 22;259(5540):224–226. doi: 10.1038/259224a0. [DOI] [PubMed] [Google Scholar]
  28. Raff M. C., Owen J. J., Cooper M. D., Lawton A. R., 3rd, Megson M., Gathings W. E. Differences in susceptibility of mature and immature mouse B lymphocytes to anti-immunoglobulin-induced immunoglobulin suppression in vitro. Possible implications for B-cell tolerance to self. J Exp Med. 1975 Nov 1;142(5):1052–1064. doi: 10.1084/jem.142.5.1052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ritter M. A., Lebacq A. M. Embryonic bursa development in vitro. Eur J Immunol. 1977 Jul;7(7):468–475. doi: 10.1002/eji.1830070713. [DOI] [PubMed] [Google Scholar]
  30. Rose M. E., Orlans E., Buttress N. Immunoglobulin classes in the hen's egg: their segregation in yolk and white. Eur J Immunol. 1974 Jul;4(7):521–523. doi: 10.1002/eji.1830040715. [DOI] [PubMed] [Google Scholar]
  31. Rose M. E., Orlans E. Normal immune responses of bursaless chickens to a secondary antigenic stimulus. Nature. 1968 Jan 20;217(5125):231–235. doi: 10.1038/217231a0. [DOI] [PubMed] [Google Scholar]
  32. Sato K., Abe S. The possible presence of a bursa-independent, IgM-producing system in chicks. Immunology. 1975 Feb;28(2):293–299. [PMC free article] [PubMed] [Google Scholar]
  33. Thorbecke G. J., Warner N. L., Hochwald G. M., Ohanian S. H. Immune globulin production by the bursa of Fabricius of young chickens. Immunology. 1968 Jul;15(1):123–134. [PMC free article] [PubMed] [Google Scholar]
  34. Vaerman J. P., Lebacq-Verheyden A. M., Heremans J. F. Absence of disulfide bridges between heavy and light chains in IgA from chicken bile. Immunol Commun. 1974;3(3):239–247. doi: 10.3109/08820137409057321. [DOI] [PubMed] [Google Scholar]

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