Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1984 Dec 1;160(6):1803–1819. doi: 10.1084/jem.160.6.1803

Cells expressing Ia antigens in the avian thymus

PMCID: PMC2187518  PMID: 6595343

Abstract

The various cell types expressing Ia antigens in the chick and quail thymus have been studied by means of monoclonal antibodies (mAb) prepared by using chick and quail thymic adherent cells (macrophages and dendritic cells) as immunogens. Three reagents were selected by the following criteria: (a) they react with a surface determinant carried by thymic adherent cells and bursal lymphocytes, (b) they can be used to immunoprecipitate from spleen cell membrane extracts molecular entities of an apparent molecular weight close to 55,000, which can be fractionated into monomers at approximately 30,000 mol wt in dissociating conditions. Among these three reagents, two are strictly species specific, i.e., they recognize either chick (TaPl) or quail (TaCl) Ia determinants, whereas the third, TaC2, recognizes both chick and quail Ia molecules. Chimeric thymuses in which the epithelioconnective stroma is derived from the quail thymic primordium and the whole hemopoietic cell population (lymphocytes and accessory cells) are of chick origin were constructed as previously described by our group (20). The different mAb were applied on normal (quail and chick) and chimeric thymuses. It appears that the thymus is divided into two compartments in terms of the nature of cells expressing Ia: the cortex, in which class II antigens are exclusively expressed by endodermal epithelial cells, and the medulla, where the majority of nonlymphoid cells are Ia-positive cells of hemopoietic origin. A few epithelial cells only are present in the thymic medulla. They are closely intricated with the sessile Ia-positive cells, whose precursors penetrate the thymus along with the lymphocyte progenitors and which are renewed in the course of thymic development. In contrast, the epithelial reticulum, expressing Ia both in the cortex and medulla, contributes a stable thymic component. During early thymic ontogeny, the hemopoietic cells expressed detectable levels of Ia antigen before the epithelial cell network.

Full Text

The Full Text of this article is available as a PDF (3.2 MB).

Selected References

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

  1. Barclay A. N., Mayrhofer G. Bone marrow origin of Ia-positive cells in the medulla rat thymus. J Exp Med. 1981 Jun 1;153(6):1666–1671. doi: 10.1084/jem.153.6.1666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bearman R. M., Levine G. D., Bensch K. G. The ultrastructure of the normal human thymus: a study of 36 cases. Anat Rec. 1978 Mar;190(3):755–781. doi: 10.1002/ar.1091900310. [DOI] [PubMed] [Google Scholar]
  3. Benacerraf B., Germain R. N. The immune response genes of the major histocompatibility complex. Immunol Rev. 1978;38:70–119. doi: 10.1111/j.1600-065x.1978.tb00385.x. [DOI] [PubMed] [Google Scholar]
  4. Cantor H., Weissman I. Development and function of subpopulations of thymocytes and T lymphocytes. Prog Allergy. 1976;20:1–64. [PubMed] [Google Scholar]
  5. Crone M., Jensenius J. C., Koch C. B-L antigens (Ia-like antigens) of the chicken major histocompatibility complex. Scand J Immunol. 1981 Dec;14(6):591–597. doi: 10.1111/j.1365-3083.1981.tb00600.x. [DOI] [PubMed] [Google Scholar]
  6. Crone M., Jensenius J., Koch C. Evidence for two populations of B-L (Ia-like) molecules encoded by the chicken MHC. Immunogenetics. 1981;13(5):381–391. doi: 10.1007/BF00346019. [DOI] [PubMed] [Google Scholar]
  7. Drews U. Cholinesterase in embryonic development. Prog Histochem Cytochem. 1975;7(3):1–52. [PubMed] [Google Scholar]
  8. Ewert D. L., Munchus M. S., Chen C. L., Cooper M. D. Analysis of structural properties and cellular distribution of avian Ia antigen by using monoclonal antibody to monomorphic determinants. J Immunol. 1984 May;132(5):2524–2530. [PubMed] [Google Scholar]
  9. Ezine S., Weissman I. L., Rouse R. V. Bone marrow cells give rise to distinct cell clones within the thymus. Nature. 1984 Jun 14;309(5969):629–631. doi: 10.1038/309629a0. [DOI] [PubMed] [Google Scholar]
  10. Fink P. J., Bevan M. J. H-2 antigens of the thymus determine lymphocyte specificity. J Exp Med. 1978 Sep 1;148(3):766–775. doi: 10.1084/jem.148.3.766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Haynes B. F., Scearce R. M., Lobach D. F., Hensley L. L. Phenotypic characterization and ontogeny of mesodermal-derived and endocrine epithelial components of the human thymic microenvironment. J Exp Med. 1984 Apr 1;159(4):1149–1168. doi: 10.1084/jem.159.4.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Janossy G., Thomas J. A., Bollum F. J., Granger S., Pizzolo G., Bradstock K. F., Wong L., McMichael A., Ganeshaguru K., Hoffbrand A. V. The human thymic microenvironment: an immunohistologic study. J Immunol. 1980 Jul;125(1):202–212. [PubMed] [Google Scholar]
  13. Jenkinson E. J., Owen J. J., Aspinall R. Lymphocyte differentiation and major histocompatibility complex antigen expression in the embryonic thymus. Nature. 1980 Mar 13;284(5752):177–179. doi: 10.1038/284177a0. [DOI] [PubMed] [Google Scholar]
  14. Jenkinson E. J., Van Ewijk W., Owen J. J. Major histocompatibility complex antigen expression on the epithelium of the developing thymus in normal and nude mice. J Exp Med. 1981 Feb 1;153(2):280–292. doi: 10.1084/jem.153.2.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jones P. P., Murphy D. B., Hewgill D., McDevitt H. O. Detection of a common polypeptide chain in I--A and I--E sub-region immunoprecipitates. Mol Immunol. 1979 Jan;16(1):51–60. doi: 10.1016/0161-5890(79)90027-0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Katz D. H. The role of the histocompatibilty gene complex in lymphocyte defferetiation. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 2):611–624. doi: 10.1101/sqb.1977.041.01.070. [DOI] [PubMed] [Google Scholar]
  18. Kaufman J. F., Auffray C., Korman A. J., Shackelford D. A., Strominger J. The class II molecules of the human and murine major histocompatibility complex. Cell. 1984 Jan;36(1):1–13. doi: 10.1016/0092-8674(84)90068-0. [DOI] [PubMed] [Google Scholar]
  19. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  20. Le Douarin N. M., Dieterlen-Lièvre F., Oliver P. D. Ontogeny of primary lymphoid organs and lymphoid stem cells. Am J Anat. 1984 Jul;170(3):261–299. doi: 10.1002/aja.1001700305. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Nowak J. S., Vainio O., Lassila O., Toivanen P., Gilmour D. G. A rosette assay for identification of Ia-like alloantigens on chicken lymphoid cells. J Immunol Methods. 1981;42(3):325–335. doi: 10.1016/0022-1759(81)90161-7. [DOI] [PubMed] [Google Scholar]
  23. Oliver P. D., LeDouarin N. M. Avian thymic accessory cells. J Immunol. 1984 Apr;132(4):1748–1755. [PubMed] [Google Scholar]
  24. Paul W. E., Benacerraf B. Functional specificity of thymus- dependent lymphocytes. Science. 1977 Mar 25;195(4284):1293–1300. doi: 10.1126/science.320663. [DOI] [PubMed] [Google Scholar]
  25. Peault B. M., Thiery J. P., Le Douarin N. M. Surface marker for hemopoietic and endothelial cell lineages in quail that is defined by a monoclonal antibody. Proc Natl Acad Sci U S A. 1983 May;80(10):2976–2980. doi: 10.1073/pnas.80.10.2976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Peault B., Coltey M., Le Douarin N. M. Tissue distribution and ontogenetic emergence of differentiation antigens on avian T cells. Eur J Immunol. 1982 Dec;12(12):1047–1050. doi: 10.1002/eji.1830121211. [DOI] [PubMed] [Google Scholar]
  27. Peck R., Murthy K. K., Vainio O. Expression of B-L (Ia-like) antigens on macrophages from chicken lymphoid organs. J Immunol. 1982 Jul;129(1):4–5. [PubMed] [Google Scholar]
  28. Robinson J. H. The ontogeny of antigen-presenting cells in fetal thymus evaluated by MLR stimulation. J Immunol. 1983 Apr;130(4):1592–1595. [PubMed] [Google Scholar]
  29. Rouse R. V., Weissman I. L. Microanatomy of the thymus: its relationship to T cell differentiation. Ciba Found Symp. 1981;84:161–177. doi: 10.1002/9780470720660.ch9. [DOI] [PubMed] [Google Scholar]
  30. Rouse R. V., van Ewijk W., Jones P. P., Weissman I. L. Expression of MHC antigens by mouse thymic dendritic cells. J Immunol. 1979 Jun;122(6):2508–2515. [PubMed] [Google Scholar]
  31. Schou M., Crone M., Simonsen M. The major histocompatibility complex of outbred chickens. I. Analysis of the B13 haplotype by serology and cellular reactions. Tissue Antigens. 1982 Nov;20(5):309–319. doi: 10.1111/j.1399-0039.1982.tb02246.x. [DOI] [PubMed] [Google Scholar]
  32. Simonsen M., Crone M., Koch C., Hála K. The MHC haplotypes of the chicken. Immunogenetics. 1982;16(6):513–532. doi: 10.1007/BF00372021. [DOI] [PubMed] [Google Scholar]
  33. Steinman R. M., Cohn Z. A. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med. 1973 May 1;137(5):1142–1162. doi: 10.1084/jem.137.5.1142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Steinman R. M., Cohn Z. A. Identification of a novel cell type in peripheral lymphoid organs of mice. II. Functional properties in vitro. J Exp Med. 1974 Feb 1;139(2):380–397. doi: 10.1084/jem.139.2.380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Van Ewijk W., Rouse R. V., Weissman I. L. Distribution of H-2 microenvironments in the mouse thymus. Immunoelectron microscopic identification of I-A and H-2K bearing cells. J Histochem Cytochem. 1980 Oct;28(10):1089–1099. doi: 10.1177/28.10.6999083. [DOI] [PubMed] [Google Scholar]
  36. Waldmann H., Pope H., Brent L., Bighouse K. Influence of the major histocompatibility complex on lymphocyte interactions in antibody formation. Nature. 1978 Jul 13;274(5667):166–168. doi: 10.1038/274166a0. [DOI] [PubMed] [Google Scholar]
  37. Waldmann H. The influence of the major histocompatibility complex on the function of T-helper cells in antibody formation. Immunol Rev. 1978;42:202–223. doi: 10.1111/j.1600-065x.1978.tb00263.x. [DOI] [PubMed] [Google Scholar]
  38. Wong T. W., Klinkert W. E., Bowers W. E. Immunological properties of thymus cell subpopulations: rat thymic dendritic cells are potent accessory cells and stimulators in a mixed leukocyte culture. Immunobiology. 1982 Feb;160(5):413–423. doi: 10.1016/S0171-2985(82)80005-3. [DOI] [PubMed] [Google Scholar]
  39. Ziegler A., Pink R. Chemical properties of two antigens controlled by the major histocompatibility complex of the chicken. J Biol Chem. 1976 Sep 10;251(17):5391–5396. [PubMed] [Google Scholar]
  40. Zinkernagel R. M., Althage A., Waterfield E., Kindred B., Welsh R. M., Callahan G., Pincetl P. Restriction specificities, alloreactivity, and allotolerance expressed by T cells from nude mice reconstituted with H-2-compatible or -incompatible thymus grafts. J Exp Med. 1980 Feb 1;151(2):376–399. doi: 10.1084/jem.151.2.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Zinkernagel R. M., Callahan G. N., Althage A., Cooper S., Klein P. A., Klein J. On the thymus in the differentiation of "H-2 self-recognition" by T cells: evidence for dual recognition? J Exp Med. 1978 Mar 1;147(3):882–896. doi: 10.1084/jem.147.3.882. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES