Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1966 Jan 1;123(1):75–102. doi: 10.1084/jem.123.1.75

THE FUNCTIONS OF THE THYMUS SYSTEM AND THE BURSA SYSTEM IN THE CHICKEN

Max D Cooper 1, Raymond D A Peterson 1, Mary Ann South 1, Robert A Good 1
PMCID: PMC2138128  PMID: 5323079

Abstract

The bursa of Fabricius and the thymus are "central lymphoid organs" in the chicken, essential to the ontogenetic development of adaptive immunity in that species. Surgical removal of one or both of these organs in the newly hatched chicken, followed by sublethal X-irradiation the next day, has permitted recognition of two morphologically distinct cell systems in the "peripheral lymphoid tissues" of the spleen, gut, and other organs, and clear definition of the separate functions of each cell system. The thymus-dependent development is represented morphologically by the small lymphocytes of the circulation and the white pulp type of development in the tissues. As in mammals, the thymus-dependent tissues of the chicken are basic to the ontogenesis of cellular immunity: graft versus host reactions, responses of delayed hypersensitivity and homograft rejection; and play a less clearly defined role in the antibody response to at least some antigens. Thymectomized-irradiated chickens are deficient in all these responses, and grow more slowly than any of the other experimental groups. In these animals germinal centers, plasma cells, and capacity for immunoglobulin synthesis remain intact. The bursa-dependent development is represented morphologically by the larger lymphocytes of the germinal centers and the plasma cells, and functionally by the immunoglobulins. Bursectomized-irradiated chickens are agammaglobulinemic and unable to produce detectable antibody despite intense, repeated stimulation with bovine serum albumin and Brucella abortus organisms. The thymus-dependent development in these animals seems to be normal; they have adequate numbers of lymphocytes in the circulation and tissues, are able to reject skin homografts, though more slowly than usual, and to exercise graft versus host reactions. The short life span of these chickens has precluded adequate study of responses of delayed hypersensitivity. There was no evidence of significant impairment of reticuloendothelial function in either the bursectomized-irradiated or the thymectomized-irradiated group, as judged by the clearance of colloidal gold and I131-tagged keyhole limpet hemocyanin.

Full Text

The Full Text of this article is available as a PDF (2.3 MB).

Selected References

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

  1. ALLIBONE E. C., GOLDIE W., MARMION B. P. PNEUMOCYSTIS CARINII PENUMONIA AND PROGRESSIVE VACCINIA IN SIBLINGS. Arch Dis Child. 1964 Feb;39:26–34. doi: 10.1136/adc.39.203.26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. ARNASON B. G., JANKOVIC B. D., WAKSMAN B. H., WENNERSTEN C. Role of the thymus in immune reactions in rats. II. Suppressive effect of thymectomy at birth on reactions of delayed (cellular) hypersensitivity and the circulating small lymphocyte. J Exp Med. 1962 Aug 1;116:177–186. doi: 10.1084/jem.116.2.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. ASPINALL R. L., MEYER R. K., GRAETZER M. A., WOLFE H. R. EFFECT OF THYMECTOMY AND BURSECTOMY ON THE SURVIVAL OF SKIN HOMOGRAFTS IN CHICKENS. J Immunol. 1963 Jun;90:872–877. [PubMed] [Google Scholar]
  4. BRUTON O. C. Agammaglobulinemia. Pediatrics. 1952 Jun;9(6):722–728. [PubMed] [Google Scholar]
  5. CANNON J. A., LONGMIRE W. P., Jr Studies of successful skin homografts in the chicken; description of a method of grafting and its application as a technic of investigation. Ann Surg. 1952 Jan;135(1):60–68. doi: 10.1097/00000658-195201000-00008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. COCK A. G., SIMONSEN M. Immunological attack on newborn chickens by injected adult cells. Immunology. 1958 Apr;1(2):103–110. [PMC free article] [PubMed] [Google Scholar]
  7. COOPER M. D., PETERSON R. D., GOOD R. A. DELINEATION OF THE THYMIC AND BURSAL LYMPHOID SYSTEMS IN THE CHICKEN. Nature. 1965 Jan 9;205:143–146. doi: 10.1038/205143a0. [DOI] [PubMed] [Google Scholar]
  8. DALMASSO A. P., MARTINEZ C., SJODIN K., GOOD R. A. STUDIES ON THE ROLE OF THE THYMUS IN IMMUNOBIOLOGY; RECONSTITUTION OF IMMUNOLOGIC CAPACITY IN MICE THYMECTOMIZED AT BIRTH. J Exp Med. 1963 Dec 1;118:1089–1109. doi: 10.1084/jem.118.6.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fahey J. L., Barth W. F., Law L. W. Normal immunoglobulins and antibody response in neonatally thymectomized mice. J Natl Cancer Inst. 1965 Oct;35(4):663–678. [PubMed] [Google Scholar]
  10. GLANZMANN E., RINIKER P. Essentielle Lymphocytophthise; ein neues Krankheitsbild aus der Säuglingspathologie. Ann Paediatr. 1950 Jul-Aug;175(1-2):1–32. [PubMed] [Google Scholar]
  11. GOOD R. A. Absence of plasma cells from bone marrow and lymph nodes following antigenic stimulation in patients with a gamma globulinemia. Rev Hematol. 1954;9(3 BIS):502–503. [PubMed] [Google Scholar]
  12. GOOD R. A., DALMASSO A. P., MARTINEZ C., ARCHER O. K., PIERCE J. C., PAPERMASTER B. W. The role of the thymus in development of immunologic capacity in rabbits and mice. J Exp Med. 1962 Nov 1;116:773–796. doi: 10.1084/jem.116.5.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GOOD R. A. Studies on agammaglobulinemia. II. Failure of plasma cell formation in the bone marrow and lymph nodes of patients with agammaglobulinemia. J Lab Clin Med. 1955 Aug;46(2):167–181. [PubMed] [Google Scholar]
  14. GORDON J., ROSE B., SEHON A. H. Detection of non-precipitating antibodies in sera of individuals allergic to ragweed pollen by an in vitro method. J Exp Med. 1958 Jul 1;108(1):37–51. doi: 10.1084/jem.108.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. GRAETZER M. A., WOLFE H. R., ASPINALL R. L., MEYER R. K. EFFECT OF THYMECTOMY AND BURSECTOMY ON PRECIPITIN AND NATURAL HEMAGGLUTININ PRODUCTION IN THE CHICKEN. J Immunol. 1963 Jun;90:878–887. [PubMed] [Google Scholar]
  16. HESS M. W., COTTIER H., STONER R. D. PRIMARY AND SECONDARY ANTITOXIN RESPONSES IN THYMECTOMIZED MICE. J Immunol. 1963 Sep;91:425–430. doi: 10.2172/4122992. [DOI] [PubMed] [Google Scholar]
  17. HONG R., SCHUBERT W. K., PERRIN E. V., WEST C. D. Antibody deficiency syndrome associated with beta-2 macroglobulinemia. J Pediatr. 1962 Dec;61:831–842. doi: 10.1016/s0022-3476(62)80193-0. [DOI] [PubMed] [Google Scholar]
  18. HUMPHREY J. H., PARROTT D. M., EAST J. STUDIES ON GLOBULIN AND ANTIBODY PRODUCTION IN MICE THYMECTOMIZED AT BIRTH. Immunology. 1964 Jul;7:419–439. [PMC free article] [PubMed] [Google Scholar]
  19. JANKOVIC B. D., LESKOWITZ S. RESTORATION OF ANTIBODY PRODUCING CAPACITY IN BURSECTOMIZED CHICKENS BY BURSAL GRAFTS IN MILLIPORE CHAMBERS. Proc Soc Exp Biol Med. 1965 Apr;118:1164–1166. doi: 10.3181/00379727-118-30070. [DOI] [PubMed] [Google Scholar]
  20. JANKOVIC B. D., WAKSMAN B. H., ARNASON B. G. Role of the thymus in immune ractions in rats. I. The immunologic response to bovine serum albumin (antibody formation, Arthus reactivity, and delayed hypersensitivity) in rats thymectomized or splenectomized at various times after birth. J Exp Med. 1962 Aug 1;116:159–176. doi: 10.1084/jem.116.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. LEVEY R. H., TRAININ N., LAW L. W. EVIDENCE FOR FUNCTION OF THYMIC TISSUE IN DIFFUSION CHAMBERS IMPLANTED IN NEONATALLY THYMECTOMIZED MICE. PRELIMINARY REPORT. J Natl Cancer Inst. 1963 Aug;31:199–217. [PubMed] [Google Scholar]
  22. MARTINEZ C., KERSEY J., PAPERMASTER B. W., GOOD R. A. Skin homograft survival in thymectomized mice. Proc Soc Exp Biol Med. 1962 Jan;109:193–196. doi: 10.3181/00379727-109-27149. [DOI] [PubMed] [Google Scholar]
  23. MCINTIRE K. R., SELL S., MILLER J. F. PATHOGENESIS OF THE POST-NEONATAL THYMECTOMY WASTING SYNDROME. Nature. 1964 Oct 10;204:151–155. doi: 10.1038/204151a0. [DOI] [PubMed] [Google Scholar]
  24. MUELLER A. P., WOLFE H. R., MEYER R. K., ASPINALL R. L. Further studies on the role of the bursa of Fabricius in antibody production. J Immunol. 1962 Mar;88:354–360. [PubMed] [Google Scholar]
  25. MUELLER A. P., WOLFE H. R., MEYER R. K. Precipitin production in chickens. XXI. Antibody production in bursectomized chickens and in chickens injected with 19-nortestosterone on the fifth day of incubasion. J Immunol. 1960 Aug;85:172–179. [PubMed] [Google Scholar]
  26. MURRAY R. G., WOODS P. A. STUDIES ON THE FATE OF LYMPHOCYTES. 3. THE MIGRATION AND METAMORPHOSIS OF IN SITU LABELED THYMIC LYMPHOCYTES. Anat Rec. 1964 Oct;150:113–128. doi: 10.1002/ar.1091500203. [DOI] [PubMed] [Google Scholar]
  27. NEZELOF C., JAMMET M. L., LORTHOLARY P., LABRUNE B., LAMY M. L'HYPOPLASIE HEREDITAIRE DU THYMUS: SA PLACE ET SA RESPONSABILITE DANS UNE OBSERVATION D'APLASIE LYMPHOCYTAIRE, NORMOPLASMOCYTAIRE ET NORMOGLOBULINEMIQUE DU NOURRISSON. Arch Fr Pediatr. 1964 Oct;21:897–920. [PubMed] [Google Scholar]
  28. NOSSAL G. J. STUDIES ON THE RATE OF SEEDING OF LYMPHOCYTES FROM THE INTACT GUINEA PIG THYMUS. Ann N Y Acad Sci. 1964 Nov 30;120:171–181. doi: 10.1111/j.1749-6632.1964.tb34715.x. [DOI] [PubMed] [Google Scholar]
  29. OPSTAD A. M. A methyl green-pyronin stain for plasma cells in tissues. Stain Technol. 1959 Sep;34:293–293. [PubMed] [Google Scholar]
  30. OSOBA D., MILLER J. F. EVIDENCE FOR A HUMORAL THYMUS FACTOR RESPONSIBLE FOR THE MATURATION OF IMMUNOLOGICAL FACULTY. Nature. 1963 Aug 17;199:653–654. doi: 10.1038/199653a0. [DOI] [PubMed] [Google Scholar]
  31. OSOBA D., MILLER J. F. THE LYMPHOD TISSUES AND IMMUNE RESPONSES OF NEONATALLY THYMECTOMIZED MICE BEARING THYMUS TISSUE IN MILLIPORE DIFFUSION CHAMBERS. J Exp Med. 1964 Jan 1;119:177–194. doi: 10.1084/jem.119.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. PAPERMASTER B. W., BRADLEY S. G., WATSON D. W., GOOD R. A. Antibody-producing capacity of adult chicken spleen cells in newly hatched chicks. J Exp Med. 1962 Jun 1;115:1191–1210. doi: 10.1084/jem.115.6.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. PETERSON R. D., BURMESTER B. R., FREDRICKSON T. N., PURCHASE H. G., GOOD R. A. EFFECT OF BURSECTOMY AND THYMECTOMY ON THE DEVELOPMENT OF VISCERAL LYMPHOMATOSIS IN THE CHICKEN. J Natl Cancer Inst. 1964 Jun;32:1343–1354. doi: 10.1093/jnci/32.6.1343. [DOI] [PubMed] [Google Scholar]
  34. ROSEN F. S., KEVY S. V., MERLER E., JANEWAY C. A., GITLIN D. Recurrent bacterial infections and dysgamma-globulinemia: deficiency of 7S gamma-globulins in the presence of elevated 19S gamma-globulins. Report of two cases. Pediatrics. 1961 Aug;28:182–195. [PubMed] [Google Scholar]
  35. Rowley D., Thöni M., Isliker H. Opsonic requirements for bacterial phagocytosis. Nature. 1965 Jul 10;207(993):210–211. doi: 10.1038/207210a0. [DOI] [PubMed] [Google Scholar]
  36. SAHIAR K., SCHWARTZ R. S. INHIBITION OF 19S ANTIBODY SYNTHESIS BY 7S ANTIBODY. Science. 1964 Jul 24;145(3630):395–397. doi: 10.1126/science.145.3630.395. [DOI] [PubMed] [Google Scholar]
  37. SIMONSEN M. The impact on the developing embryo and newborn animal of adult homologous cells. Acta Pathol Microbiol Scand. 1957;40(6):480–500. [PubMed] [Google Scholar]
  38. STPIERRE R. L., ACKERMAN G. A. BURSA OF FABRICIUS IN CHICKENS: POSSIBLE HUMORAL FACTOR. Science. 1965 Mar 12;147(3663):1307–1308. doi: 10.1126/science.147.3663.1307. [DOI] [PubMed] [Google Scholar]
  39. Smithies O. Antibody Induction and Tolerance. Science. 1965 Jul 9;149(3680):151–156. doi: 10.1126/science.149.3680.151. [DOI] [PubMed] [Google Scholar]
  40. Sutherland D. E., Archer O. K., Peterson R. D., Eckert E., Good R. A. Development of "autoimmune processes" in rabbits after neonatal removal of central lymphoid tissue. Lancet. 1965 Jan 16;1(7377):130–133. doi: 10.1016/s0140-6736(65)91091-3. [DOI] [PubMed] [Google Scholar]
  41. TALMAGE D. W., DIXON F. J., BUKANTZ S. C., DAMMIN G. J. Antigen elimination from the blood as an early manifestation of the immune response. J Immunol. 1951 Oct;67(4):243–255. [PubMed] [Google Scholar]
  42. TANNER J. M. The measurement of body fat in man. Proc Nutr Soc. 1959;18:148–155. doi: 10.1079/pns19590038. [DOI] [PubMed] [Google Scholar]
  43. TOBLER R., COTTIER H. Familiäre Lymphopenie mit Agammaglobulinämie und schwerer Moniliasis: die essentielle Lymphocytophthise als besondere Form der frühkindlichen Agammaglobulinamie. Helv Paediatr Acta. 1958 Oct;13(4):313–338. [PubMed] [Google Scholar]
  44. 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]

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

RESOURCES