Skip to main content
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1976 Nov 2;144(5):1254–1262. doi: 10.1084/jem.144.5.1254

Allogeneic carrier-specific enhancement of hapten-specific secondary B- cell responses

PMCID: PMC2190464  PMID: 1086883

Abstract

We have analyzed the capacity of carrier-specific T cells to enhance the immune response of hapten-specific secondary B cells which do not share genes in the H-2 complex with the T cells. For this analysis we have used the in vitro splenic focus technique which allows assessment of monoclonal responses of B cells isolated in splenic fragment cultures of irradiated reconstituted carrier primed mice. A previous report from this laboratory demonstrated that syngeny in the I region of the H-2 complex was necessary between collaborating hapten-specific primary (nonimmune) B cells and carrier-specific T cells for responses yielding IgG1 but not IgM antibody. These findings lead up to postulate that the expression of I-region gene products on the surface of primary B cells and I-region syngeny with collaborating carrier-specific T cells were essential elements in the triggering events leading to IgG1 synthesis by primary B cells. The results presented in the present report indicate that, unlike primary B cells, the majority of secondary B cells can be stimulated to produce IgG1 antibody in carrier-primed allogeneic recipients. Although the enhancement of secondary IgG1 responses is slightly greater with syngeneic T cells, the allogeneic collaborative interaction requires both carrier priming of recipient mice and stimulation with the homologous hapten-carrier complex and thus appears to be specific. These findings clearly discriminate secondary from primary B cells and indicate that the mechanism of stimulation of secondary B cells to yield IgG1-producing clones differs fundamentally from the stimulation of primary B cells in that the requisite for I-region syngeny is obviated.

Full Text

The Full Text of this article is available as a PDF (603.6 KB).

Selected References

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

  1. Armerding D., Sachs D. H., Katz D. H. Activation of T and B lymphocytes in vitro. III. Presence of Ia determinants on allogeneic effect factor. J Exp Med. 1974 Dec 1;140(6):1717–1722. doi: 10.1084/jem.140.6.1717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Askenase P. W., Leonard E. J. Solid phase radioimmunoassay of human beta 1C globulin. Immunochemistry. 1970 Jan;7(1):29–41. doi: 10.1016/0019-2791(70)90028-5. [DOI] [PubMed] [Google Scholar]
  3. Bach F. H., Segall M., Zier K. S., Sondel P. M., Alter B. J., Bach M. L. Cell mediated immunity: separation of cells involved in recognitive and destructive phases. Science. 1973 Apr 27;180(4084):403–406. doi: 10.1126/science.180.4084.403. [DOI] [PubMed] [Google Scholar]
  4. Bechtol K. B., Freed J. H., Herzenberg L. A., McDevitt H. O. Genetic control of the antibody response to poly-L(Tyr,Glu)-poly-D,L-Ala--poly-L-Lys in C3H--CWB tetraparental mice. J Exp Med. 1974 Dec 1;140(6):1660–1675. doi: 10.1084/jem.140.6.1660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bechtol K. B., McDevitt H. O. Antibody response of C3H in equilibrium (CKB X CWB)F1 tetraparental mice to poly-L(Tyr,Glu)-poly-D,L-Ala-poly-L-Lys immunization. J Exp Med. 1976 Jul 1;144(1):123–144. doi: 10.1084/jem.144.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benacerraf B., McDevitt H. O. Histocompatibility-linked immune response genes. Science. 1972 Jan 21;175(4019):273–279. doi: 10.1126/science.175.4019.273. [DOI] [PubMed] [Google Scholar]
  7. Braley-Mullen H. Secondary IgG responses to type III pneumococcal polysaccharide. I. Kinetics and antigen requirements. J Immunol. 1975 Nov;115(5):1194–1198. [PubMed] [Google Scholar]
  8. Erb P., Feldmann M. The role of macrophages in the generation of T-helper cells. II. The genetic control of the macrophage-T-cell interaction for helper cell induction with soluble antigens. J Exp Med. 1975 Aug 1;142(2):460–472. doi: 10.1084/jem.142.2.460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gearhart P. J., Sigal N. H., Klinman N. R. Production of antibodies of identical idiotype but diverse immunoglobulin classes by cells derived from a single stimulated B cell. Proc Natl Acad Sci U S A. 1975 May;72(5):1707–1711. doi: 10.1073/pnas.72.5.1707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Janeway C. A., Jr Cellular cooperation during in vivo anti-hapten antibody responses. I. The effect of cell number on the response. J Immunol. 1975 Apr;114(4):1394–1401. [PubMed] [Google Scholar]
  11. Katz D. H., Benacerraf B. The function and interrelationships of T-cell receptors, Ir genes and other histocompatibility gene products. Transplant Rev. 1975;22:175–195. doi: 10.1111/j.1600-065x.1975.tb01559.x. [DOI] [PubMed] [Google Scholar]
  12. Klaus G. G., Humphrey J. H. B cell tolerance induced by polymeric antigens. I. Comparison of the dose and epitope density requirements for inactivation of primed and unprimed B cells in vivo. Eur J Immunol. 1976 Jun;5(6):361–365. doi: 10.1002/eji.1830050602. [DOI] [PubMed] [Google Scholar]
  13. Klinman N. R., Pickard A. R., Sigal N. H., Gearhart P. J., Metcalf E. S., Pierce S. K. Assessing B cell diversification by antigen receptor and precursor cell analysis. Ann Immunol (Paris) 1976 Jun-Jul;127(3-4):489–502. [PubMed] [Google Scholar]
  14. Klinman N. R., Press J. L., Segal G. P. Overlap stimulation of primary and secondary B cells by cross-reacting determinants. J Exp Med. 1973 Nov 1;138(5):1276–1281. doi: 10.1084/jem.138.5.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Klinman N. R., Press J. L. The B cell specificity repertoire: its relationship to definable subpopulations. Transplant Rev. 1975;24:41–83. doi: 10.1111/j.1600-065x.1975.tb00165.x. [DOI] [PubMed] [Google Scholar]
  16. Klinman N. R. The mechanism of antigenic stimulation of primary and secondary clonal precursor cells. J Exp Med. 1972 Aug 1;136(2):241–260. doi: 10.1084/jem.136.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lieberman R., Potter M., Mushinski E. B., Humphrey W., Jr, Rudikoff S. Genetics of a new IgVH (T15 idiotype) marker in the mouse regulating natural antibody to phosphorylcholine. J Exp Med. 1974 Apr 1;139(4):983–1001. doi: 10.1084/jem.139.4.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pierce C. W., Kapp J. A., Benacerraf B. Regulation by the H-2 gene complex of macrophage-lymphoid cell interactions in secondary antibody responses in vitro. J Exp Med. 1976 Aug 1;144(2):371–381. doi: 10.1084/jem.144.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pierce C. W., Solliday S. M., Asofsky R. Immune responses in vitro. V. Suppression of M, G, and A plaque-forming cell responses in cultures of primed mouse spleen cells by class-specific antibody to mouse immunoglobulins. J Exp Med. 1972 Mar 1;135(3):698–710. doi: 10.1084/jem.135.3.698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pierce S. K., Klinman N. R. The allogeneic bisection of carrier-specific enhancement of monoclonal B-cell responses. J Exp Med. 1975 Nov 1;142(5):1165–1179. doi: 10.1084/jem.142.5.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Press J. L., Klinman N. R., McDevitt H. O. Expression of Ia antigens on hapten-specific B cells. I. Delineation of B-cell subpopulations. J Exp Med. 1976 Aug 1;144(2):414–427. doi: 10.1084/jem.144.2.414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sher A., Cohn M. Inheritance of an idiotype associated with the immune response of inbred mice to phosphorylcholine. Eur J Immunol. 1972 Aug;2(4):319–326. doi: 10.1002/eji.1830020405. [DOI] [PubMed] [Google Scholar]
  23. Strober S. Immune function cell surface characteristics and maturation of B cell subpopulations. Transplant Rev. 1975;24:84–112. doi: 10.1111/j.1600-065x.1975.tb00166.x. [DOI] [PubMed] [Google Scholar]
  24. Taussig M. J., Munro A. J., Campbell R., David C. S., Staines N. A. Antigen-specific T-cell factor in cell cooperation. Mapping within the I region of the H-2 complex and ability to cooperate across allogeneic barriers. J Exp Med. 1975 Sep 1;142(3):694–700. doi: 10.1084/jem.142.3.694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. von Boehmer H., Hudson L., Sprent J. Collaboration of histoincompatible T and B lymphocytes using cells from tetraparental bone marrow chimeras. J Exp Med. 1975 Oct 1;142(4):989–997. doi: 10.1084/jem.142.4.989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES