Skip to main content
NCBI home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1971 Jul 1;134(1):103–119. doi: 10.1084/jem.134.1.103

THE RELATIONSHIP BETWEEN ANTIGENIC STRUCTURE AND THE REQUIREMENT FOR THYMUS-DERIVED CELLS IN THE IMMUNE RESPONSE

Marc Feldmann 1, Antony Basten 1
PMCID: PMC2139040  PMID: 4104294

Abstract

Certain antigens such as polymerized flagellin are capable of producing relatively normal antibody levels in thymectomized mice, whereas others, including heterologous erythrocytes require the presence of T cells in a helper capacity. The mechanism of thymus-independent antibody production was investigated by comparing the primary IgM responses of spleen cells from ATXBM, XBM, and normal mice to various physical forms of the flagellar antigens of Salmonella adelaide in vitro. No reduction in antibody-forming cell levels to polymerized flagellin over a wide dose range was observed in ATXBM cultures, although the same spleen cells did not respond to an optimal dose of sheep red cells. In contrast, when flagellar determinants were presented in a monomeric form or as flagellin-coated donkey red cells, a highly significant difference was observed between the antibody responses of spleen cells from ATXBM mice and XBM or normal controls. The results suggested that the requirement for T cells in antibody production is not a property of specific antigenic determinants, but depends on the mode of antigenic presentation. The validity of this conclusion was confirmed by using another antigenic determinant (DNP) coupled either to the thymus-independent carrier, POL, or to the thymus-dependent carrier, DRC. Spleen cells from XBM mice produced comparable AFC levels to both forms of DNP, but the results from ATXBM cultures showed a marked difference. The anti-DNP response to DNP-DRC was greatly reduced compared to controls, whereas that to DNP-POL was normal even after prolonged thoracic duct drainage of the ATXBM donors and pretreatment of their spleen cells with anti-θ-serum and complement. The data presented here imply that the role of T cells in humoral immunity is the presentation of antigen to B cells in such a manner as to initiate optimal antibody synthesis.

Full Text

The Full Text of this article is available as a PDF (920.3 KB).

Selected References

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

  1. ADA G. L., NOSSAL G. J., PYE J., ABBOT A. ANTIGENS IN IMMUNITY. I. PREPARATION AND PROPERTIES OF FLAGELLAR ANTIGENS FROM SALMONELLA ADELAIDE. Aust J Exp Biol Med Sci. 1964 Jun;42:267–282. [PubMed] [Google Scholar]
  2. Basch R. S. Immunologic competence after thymectomy. Int Arch Allergy Appl Immunol. 1966;30(2):105–119. doi: 10.1159/000229800. [DOI] [PubMed] [Google Scholar]
  3. CROSS A. M., LEUCHARS E., DAVIES A. J. RETENTION OF IMMUNOLOGICAL INFORMATION. (II). BY THYMECTOMIZED SYNGENEIC RADIATION CHIMAERAS. Nature. 1964 Sep 5;203:1042–1045. doi: 10.1038/2031042a0. [DOI] [PubMed] [Google Scholar]
  4. Cohen A., Schlesinger M. Absorption of guinea pig serum with agar. A method for elimination of itscytotoxicity for murine thymus cells. Transplantation. 1970 Jul;10(1):130–132. doi: 10.1097/00007890-197007000-00027. [DOI] [PubMed] [Google Scholar]
  5. Cunningham A. J., Szenberg A. Further improvements in the plaque technique for detecting single antibody-forming cells. Immunology. 1968 Apr;14(4):599–600. [PMC free article] [PubMed] [Google Scholar]
  6. Davies A. J., Carter R. L., Leuchars E., Wallis V., Dietrich F. M. The morphology of immune reactions in normal, thymectomized and reconstituted mice. 3. Response to bacterial antigens: salmonellar flagellar antigen and pneumococcal plysaccharide. Immunology. 1970 Dec;19(6):945–957. [PMC free article] [PubMed] [Google Scholar]
  7. Diener E. A new method for the enumeration of single antibody-producing cells. J Immunol. 1968 May;100(5):1062–1070. [PubMed] [Google Scholar]
  8. Diener E., Feldmann M. Antibody-mediated suppression of the immune response in vitro. II. A new approach to the phenomenon of immunological tolerance. J Exp Med. 1970 Jul 1;132(1):31–43. doi: 10.1084/jem.132.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. HANKS J. H., WALLACE J. H. Determination of cell viability. Proc Soc Exp Biol Med. 1958 May;98(1):188–192. doi: 10.3181/00379727-98-23985. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. JERNE N. K., NORDIN A. A. Plaque formation in agar by single antibody-producing cells. Science. 1963 Apr 26;140(3565):405–405. [PubMed] [Google Scholar]
  14. Katz D. H., Paul W. E., Goidl E. A., Benacerraf B. Carrier function in anti-hapten immune responses. I. Enhancement of primary and secondary anti-hapten antibody responses by carrier preimmunization. J Exp Med. 1970 Aug 1;132(2):261–282. doi: 10.1084/jem.132.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. LOWY J., HANSON J. ELECTRON MICROSCOPE STUDIES OF BACTERIAL FLAGELLA. J Mol Biol. 1965 Feb;11:293–313. doi: 10.1016/s0022-2836(65)80059-6. [DOI] [PubMed] [Google Scholar]
  16. Miller J. F., De Burgh P. M., Grant G. A. Thymus and the production of antibody-plaque-forming cells. Nature. 1965 Dec 25;208(5017):1332–1334. doi: 10.1038/2081332a0. [DOI] [PubMed] [Google Scholar]
  17. Miller J. F., Mitchell G. F. Cell to cell interaction in the immune response. I. Hemolysin-forming cells in neonatally thymectomized mice reconstituted with thymus or thoracic duct lymphocytes. J Exp Med. 1968 Oct 1;128(4):801–820. doi: 10.1084/jem.128.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Miller J. F., Mitchell G. F. Thymus and antigen-reactive cells. Transplant Rev. 1969;1:3–42. doi: 10.1111/j.1600-065x.1969.tb00135.x. [DOI] [PubMed] [Google Scholar]
  19. Miller J. F., Osoba D. Current concepts of the immunological function of the thymus. Physiol Rev. 1967 Jul;47(3):437–520. doi: 10.1152/physrev.1967.47.3.437. [DOI] [PubMed] [Google Scholar]
  20. Miller J. F., Sprent J. Thymus-derived cells in mouse thoracic duct lymph. Nat New Biol. 1971 Apr 28;230(17):267–270. doi: 10.1038/newbio230267a0. [DOI] [PubMed] [Google Scholar]
  21. Paul W. E., Katz D. H., Goidl E. A., Benacerraf B. Carrier function in anti-hapten immune responses. II. Specific properties of carrier cells capable of enhancing anti-hapten antibody responses. J Exp Med. 1970 Aug 1;132(2):283–299. doi: 10.1084/jem.132.2.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Perucca P. J., Faulk W. P., Fudenberg H. H. Passive immune lysis with chromic chloride-treated erythrocytes. J Immunol. 1969 Apr;102(4):812–820. [PubMed] [Google Scholar]
  23. REIF A. E., ALLEN J. M. THE AKR THYMIC ANTIGEN AND ITS DISTRIBUTION IN LEUKEMIAS AND NERVOUS TISSUES. J Exp Med. 1964 Sep 1;120:413–433. doi: 10.1084/jem.120.3.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Raff M. C., Wortis H. H. Thymus dependence of theta-bearing cells in the peripheral lymphoid tissues of mice. Immunology. 1970 Jun;18(6):931–942. [PMC free article] [PubMed] [Google Scholar]
  25. Sinclair N. R., Elliott E. V. Neonatal thymectomy and the decrease in antigen-sensitivity of the primary response and immunological "memory" systems. Immunology. 1968 Sep;15(3):325–333. [PMC free article] [PubMed] [Google Scholar]
  26. Sjöberg O., Möller E. Antigen binding cells in tolerant animals. Nature. 1970 Nov 21;228(5273):780–781. doi: 10.1038/228780a0. [DOI] [PubMed] [Google Scholar]
  27. Taylor R. B. Cellular cooperation in the antibody response of mice to two serum albumins: specific function of thymus cells. Transplant Rev. 1969;1:114–149. doi: 10.1111/j.1600-065x.1969.tb00138.x. [DOI] [PubMed] [Google Scholar]
  28. Taylor R. B., Wortis H. H. Thymus dependence of antibody response: variation with dose of antigen and class of antibody. Nature. 1968 Nov 30;220(5170):927–928. doi: 10.1038/220927a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES