Emergence of committed B lymphoid progenitors in the developing chicken embryo (original) (raw)

Abstract

The formation of B lymphoid restricted progenitors was followed during chicken embryonic development by monitoring the appearance of the various Ig gene rearrangements (DJH, VHDJH, V lambda J lambda), as a sensitivity that allows the detection of a single rearranged cell. By quantifying the DJH committed progenitor populations, we describe their evolution in different compartments at different developmental stages. The yolk sac is the first site where DJH-positive cells are observed (at days 5-6 of development); via the general circulation, they then seed the various organs while undergoing VHDJH and V lambda J lambda rearrangements, which occur simultaneously but lag behind DJH by one to several days. These progenitor populations decline with time in most lymphoid sites and only expand in the bursa. RAG-1 expression is observed in the bursa in the absence of ongoing rearrangement activity and thus appears to be an improper marker of rearrangement in the chicken. Commitment to the B cell lineage seems to result from an intrinsic cell program, but the survival and expansion of the committed B progenitors require the specific microenvironment of the bursa.

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Selected References

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  1. Becker R. S., Knight K. L. Somatic diversification of immunoglobulin heavy chain VDJ genes: evidence for somatic gene conversion in rabbits. Cell. 1990 Nov 30;63(5):987–997. doi: 10.1016/0092-8674(90)90502-6. [DOI] [PubMed] [Google Scholar]
  2. Benatar T., Iacampo S., Tkalec L., Ratcliffe M. J. Expression of immunoglobulin genes in the avian embryo bone marrow revealed by retroviral transformation. Eur J Immunol. 1991 Oct;21(10):2529–2536. doi: 10.1002/eji.1830211033. [DOI] [PubMed] [Google Scholar]
  3. Born W., White J., Kappler J., Marrack P. Rearrangement of IgH genes in normal thymocyte development. J Immunol. 1988 May 1;140(9):3228–3232. [PubMed] [Google Scholar]
  4. Carlson L. M., Oettinger M. A., Schatz D. G., Masteller E. L., Hurley E. A., McCormack W. T., Baltimore D., Thompson C. B. Selective expression of RAG-2 in chicken B cells undergoing immunoglobulin gene conversion. Cell. 1991 Jan 11;64(1):201–208. doi: 10.1016/0092-8674(91)90221-j. [DOI] [PubMed] [Google Scholar]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. Coltey M., Jotereau F. V., Le Douarin N. M. Evidence for a cyclic renewal of lymphocyte precursor cells in the embryonic chick thymus. Cell Differ. 1987 Nov;22(1):71–82. doi: 10.1016/0045-6039(87)90414-3. [DOI] [PubMed] [Google Scholar]
  7. Cormier F., de Paz P., Dieterlen-Lièvre F. In vitro detection of cells with monocytic potentiality in the wall of the chick embryo aorta. Dev Biol. 1986 Nov;118(1):167–175. doi: 10.1016/0012-1606(86)90084-9. [DOI] [PubMed] [Google Scholar]
  8. Cumano A., Paige C. J. Enrichment and characterization of uncommitted B-cell precursors from fetal liver at day 12 of gestation. EMBO J. 1992 Feb;11(2):593–601. doi: 10.1002/j.1460-2075.1992.tb05091.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dieterlen-Lièvre F., Martin C. Diffuse intraembryonic hemopoiesis in normal and chimeric avian development. Dev Biol. 1981 Nov;88(1):180–191. doi: 10.1016/0012-1606(81)90228-1. [DOI] [PubMed] [Google Scholar]
  10. Dunon D., Kaufman J., Salomonsen J., Skjoedt K., Vainio O., Thiery J. P., Imhof B. A. T cell precursor migration towards beta 2-microglobulin is involved in thymus colonization of chicken embryos. EMBO J. 1990 Oct;9(10):3315–3322. doi: 10.1002/j.1460-2075.1990.tb07531.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grossi C. E., Lydyard P. M., Cooper M. D. Ontogeny of B cells in the chicken. II. Changing patterns of cytoplasmic IgM expression and of modulation requirements for surface IgM by anti-mu antibodies. J Immunol. 1977 Aug;119(2):749–756. [PubMed] [Google Scholar]
  12. Hardy R. R., Carmack C. E., Shinton S. A., Kemp J. D., Hayakawa K. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J Exp Med. 1991 May 1;173(5):1213–1225. doi: 10.1084/jem.173.5.1213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Houssaint E., Belo M., Le Douarin N. M. Investigations on cell lineage and tissue interactions in the developing bursa of Fabricius through interspecific chimeras. Dev Biol. 1976 Oct 15;53(2):250–264. doi: 10.1016/0012-1606(76)90227-x. [DOI] [PubMed] [Google Scholar]
  14. Houssaint E. Cell lineage segregation during bursa of Fabricius ontogeny. J Immunol. 1987 Jun 1;138(11):3626–3634. [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Houssaint E., Mansikka A., Vainio O. Early separation of B and T lymphocyte precursors in chick embryo. J Exp Med. 1991 Aug 1;174(2):397–406. doi: 10.1084/jem.174.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kim H. S., Smithies O. Recombinant fragment assay for gene targetting based on the polymerase chain reaction. Nucleic Acids Res. 1988 Sep 26;16(18):8887–8903. doi: 10.1093/nar/16.18.8887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kurosawa Y., von Boehmer H., Haas W., Sakano H., Trauneker A., Tonegawa S. Identification of D segments of immunoglobulin heavy-chain genes and their rearrangement in T lymphocytes. Nature. 1981 Apr 16;290(5807):565–570. doi: 10.1038/290565a0. [DOI] [PubMed] [Google Scholar]
  20. Lassila O., Eskola J., Toivanen P., Dieterlen-Lièvre F. Lymphoid stem cells in the intraembryonic mesenchyme of the chicken. Scand J Immunol. 1980;11(4):445–448. doi: 10.1111/j.1365-3083.1980.tb00011.x. [DOI] [PubMed] [Google Scholar]
  21. Lassila O., Eskola J., Toivanen P., Martin C., Dieterlen-Lievre F. The origin of lymphoid stem cells studied in chick yold sac-embryo chimaeras. Nature. 1978 Mar 23;272(5651):353–354. doi: 10.1038/272353a0. [DOI] [PubMed] [Google Scholar]
  22. Lassila O., Eskola J., Toivanen P. Prebursal stem cells in the intraembryonic mesenchyme of the chick embryo at 7 days of incubation. J Immunol. 1979 Nov;123(5):2091–2094. [PubMed] [Google Scholar]
  23. Lassila O., Martin C., Dieterlen-Lièvre F., Gilmour D. G., Eskola J., Toivanen P. Migration of prebursal stem cells from the early chicken embryo to the yolk sac. Scand J Immunol. 1982 Sep;16(3):265–268. doi: 10.1111/j.1365-3083.1982.tb00722.x. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. McCormack W. T., Tjoelker L. W., Barth C. F., Carlson L. M., Petryniak B., Humphries E. H., Thompson C. B. Selection for B cells with productive IgL gene rearrangements occurs in the bursa of Fabricius during chicken embryonic development. Genes Dev. 1989 Jun;3(6):838–847. doi: 10.1101/gad.3.6.838. [DOI] [PubMed] [Google Scholar]
  27. McCormack W. T., Tjoelker L. W., Carlson L. M., Petryniak B., Barth C. F., Humphries E. H., Thompson C. B. Chicken IgL gene rearrangement involves deletion of a circular episome and addition of single nonrandom nucleotides to both coding segments. Cell. 1989 Mar 10;56(5):785–791. doi: 10.1016/0092-8674(89)90683-1. [DOI] [PubMed] [Google Scholar]
  28. Melchers F. Murine embryonic B lymphocyte development in the placenta. Nature. 1979 Jan 18;277(5693):219–221. doi: 10.1038/277219a0. [DOI] [PubMed] [Google Scholar]
  29. Moore M. A., Owen J. J. Chromosome marker studies in the irradiated chick embryo. Nature. 1967 Sep 2;215(5105):1081–1082. doi: 10.1038/2151081a0. [DOI] [PubMed] [Google Scholar]
  30. Oettinger M. A., Schatz D. G., Gorka C., Baltimore D. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science. 1990 Jun 22;248(4962):1517–1523. doi: 10.1126/science.2360047. [DOI] [PubMed] [Google Scholar]
  31. Ogawa M., Nishikawa S., Ikuta K., Yamamura F., Naito M., Takahashi K., Nishikawa S. B cell ontogeny in murine embryo studied by a culture system with the monolayer of a stromal cell clone, ST2: B cell progenitor develops first in the embryonal body rather than in the yolk sac. EMBO J. 1988 May;7(5):1337–1343. doi: 10.1002/j.1460-2075.1988.tb02949.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Osmond D. G. Population dynamics of bone marrow B lymphocytes. Immunol Rev. 1986 Oct;93:103–124. doi: 10.1111/j.1600-065x.1986.tb01504.x. [DOI] [PubMed] [Google Scholar]
  33. Owen J. J., Raff M. C., Cooper M. D. Studies on the generation of B lymphocytes in the mouse embryo. Eur J Immunol. 1976 Jul;5(7):468–473. doi: 10.1002/eji.1830050708. [DOI] [PubMed] [Google Scholar]
  34. Palacios R., Samaridis J. Fetal liver pro-B and pre-B lymphocyte clones: expression of lymphoid-specific genes, surface markers, growth requirements, colonization of the bone marrow, and generation of B lymphocytes in vivo and in vitro. Mol Cell Biol. 1992 Feb;12(2):518–530. doi: 10.1128/mcb.12.2.518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Pink J. R., Lassila O. B-cell commitment and diversification in the bursa of Fabricius. Curr Top Microbiol Immunol. 1987;135:57–64. doi: 10.1007/978-3-642-71851-9_4. [DOI] [PubMed] [Google Scholar]
  36. Pink J. R., Ratcliffe M. J., Vainio O. Immunoglobulin-bearing stem cells for clones of B (bursa-derived) lymphocytes. Eur J Immunol. 1985 Jun;15(6):617–620. doi: 10.1002/eji.1830150616. [DOI] [PubMed] [Google Scholar]
  37. Ratcliffe M. J., Lassila O., Pink J. R., Vainio O. Avian B cell precursors: surface immunoglobulin expression is an early, possibly bursa-independent event. Eur J Immunol. 1986 Feb;16(2):129–133. doi: 10.1002/eji.1830160204. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Reynaud C. A., Anquez V., Weill J. C. The chicken D locus and its contribution to the immunoglobulin heavy chain repertoire. Eur J Immunol. 1991 Nov;21(11):2661–2670. doi: 10.1002/eji.1830211104. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. Reynaud C. A., Mackay C. R., Müller R. G., Weill J. C. Somatic generation of diversity in a mammalian primary lymphoid organ: the sheep ileal Peyer's patches. Cell. 1991 Mar 8;64(5):995–1005. doi: 10.1016/0092-8674(91)90323-q. [DOI] [PubMed] [Google Scholar]
  43. Rolink A., Kudo A., Karasuyama H., Kikuchi Y., Melchers F. Long-term proliferating early pre B cell lines and clones with the potential to develop to surface Ig-positive, mitogen reactive B cells in vitro and in vivo. EMBO J. 1991 Feb;10(2):327–336. doi: 10.1002/j.1460-2075.1991.tb07953.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Schatz D. G., Oettinger M. A., Baltimore D. The V(D)J recombination activating gene, RAG-1. Cell. 1989 Dec 22;59(6):1035–1048. doi: 10.1016/0092-8674(89)90760-5. [DOI] [PubMed] [Google Scholar]
  45. Tyan M. L., Herzenberg L. A. Studies on the ontogeny of the mouse immune system. II. Immunoglobulin-producing cells. J Immunol. 1968 Sep;101(3):446–450. [PubMed] [Google Scholar]
  46. Weill J. C., Reynaud C. A., Lassila O., Pink J. R. Rearrangement of chicken immunoglobulin genes is not an ongoing process in the embryonic bursa of Fabricius. Proc Natl Acad Sci U S A. 1986 May;83(10):3336–3340. doi: 10.1073/pnas.83.10.3336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Weill J. C., Reynaud C. A. The chicken B cell compartment. Science. 1987 Nov 20;238(4830):1094–1098. doi: 10.1126/science.3317827. [DOI] [PubMed] [Google Scholar]