Skip to main content
Immunology logoLink to Immunology
. 1973 Mar;24(3):409–424.

Antibody production in mice

V. The suppressive effect of anti-carrier antibodies on cellular cooperation in the induction of secondary anti-hapten antibody responses

T Hamaoka, K Takatsu, M Kitagawa
PMCID: PMC1422970  PMID: 4540955

Abstract

Cooperative induction of secondary anti-hapten antibody responses was studied by using non-cross-reactive carrier proteins, bacterial α-amylase (BαA), Taka-amylase A (TAA) and keyhole-limpet haemocyanin (KLH), and the 2,4-dinitrophenyl (DNP) and benzylpenicilloyl (BPO) groups as haptenic determinants.

Lymphoid cells obtained from mice primed with a hapten-carrier conjugate could be effectively stimulated with a hapten-heterologous carrier conjugate, provided that lymphoid cells primed to the heterologous carrier were also present. In the carrier-primed lymphoid cell population, helper activity of thymus-derived cells developed earlier following carrier immunization than did the capacity of antibody-forming cell precursors (AFCP) to produce an effective anti-carrier antibody response upon secondary stimulation. Attempts to generate hapten-specific helper cell activity were unsuccessful. Thus, cells primed to one haptenic determinant failed to exert a helper function with cells primed to a second hapten upon subsequent administration to the two haptens together on the same heterologous carrier molecule.

In order to distinguish among carrier determinant specificities which react with thymus-derived helper cells from those which react with bone marrow-derived AFCP, the capacity of various anti-carrier antibodies or antibody fragments to suppress either anti-carrier antibody production alone or together with helper cell function in adoptive secondary anti-hapten antibody responses was tested. In this system, it was found that 7S anti-carrier antibody suppressed the reaction of helper cells and carrier-specific AFCP such that both the anti-hapten and anti-carrier antibody responses were abrogated. By contrast, passively administered 3.5S fragments of anti-carrier antibodies selectively prevented the stimulation of carrier-specific AFCP to produce anti-carrier antibodies, but had no effect on the capacity of carrier-specific helper cells to facilitate the secondary anti-hapten antibody response. As expected, passively administered 7S anti-hapten antibodies selectively abrogated the production of anti-hapten, but not anti-carrier antibodies. These data are discussed in the context of suggesting that distinct determinant sites on carrier molecules are recognized independently by thymus-derived helper cells and by bone marrow-derived AFCP.

Full text

PDF
409

Selected References

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

  1. Ada G. L. Antigen binding cells in tolerance and immunity. Transplant Rev. 1970;5:105–129. doi: 10.1111/j.1600-065x.1970.tb00358.x. [DOI] [PubMed] [Google Scholar]
  2. Basten A., Miller J. F., Warner N. L., Pye J. Specific inactivation of thymus-derived (T) and non-thymus-derived (B) lymphocytes by 125I-labelled antigen. Nat New Biol. 1971 May 26;231(21):104–106. doi: 10.1038/newbio231104a0. [DOI] [PubMed] [Google Scholar]
  3. Celada F., Schmidt D., Strom R. Determination of avidity of anti-albumin antibodies in the mouse. Influence of the number of cells transferred on the quality of the secondary adoptive response. Immunology. 1969 Aug;17(2):189–198. [PMC free article] [PubMed] [Google Scholar]
  4. Claman H. N., Chaperon E. A. Immunologic complementation between thymus and marrow cells--a model for the two-cell theory of immunocompetence. Transplant Rev. 1969;1:92–113. doi: 10.1111/j.1600-065x.1969.tb00137.x. [DOI] [PubMed] [Google Scholar]
  5. Feldmann M., Easten A. The relationship between antigenic structure and the requirement for thymus-derived cells in the immune response. J Exp Med. 1971 Jul 1;134(1):103–119. doi: 10.1084/jem.134.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Greaves M. F. Biological effects of anti-immunoglobulins: evidence for immunoglobulin receptors on 'T' and 'B' lymphocytes. Transplant Rev. 1970;5:45–75. doi: 10.1111/j.1600-065x.1970.tb00356.x. [DOI] [PubMed] [Google Scholar]
  7. Hamaoka T., Kitagawa M. Antibody production in mice. II. The mechanism of antigenic stimulation in the secondary immune response. Immunology. 1971 Feb;20(2):191–203. [PMC free article] [PubMed] [Google Scholar]
  8. Hamaoka T., Kitagawa M., Matsuoka Y., Yamamura Y. Antibody production in mice. I. The analysis of immunological memory. Immunology. 1969 Jul;17(1):55–69. [PMC free article] [PubMed] [Google Scholar]
  9. Hamaoka T., Takatsu K., Masaki H., Matsuoka Y., Kitagawa M. Antibody production in mice. 3. The suppressive effect of antibody on the initiation of secondary immune response. Immunology. 1971 Jun;20(6):871–881. [PMC free article] [PubMed] [Google Scholar]
  10. Katz D. H., Benacerraf B. The regulatory influence of activated T cells on B cell responses to antigen. Adv Immunol. 1972;15:1–94. doi: 10.1016/s0065-2776(08)60683-5. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Mitchison N. A. The carrier effect in the secondary response to hapten-protein conjugates. II. Cellular cooperation. Eur J Immunol. 1971 Jan;1(1):18–27. doi: 10.1002/eji.1830010104. [DOI] [PubMed] [Google Scholar]
  14. Mitchison N. A. The carrier effect in the secondary response to hapten-protein conjugates. V. Use of antilymphocyte serum to deplete animals of helper cells. Eur J Immunol. 1971 Apr;1(2):68–75. doi: 10.1002/eji.1830010204. [DOI] [PubMed] [Google Scholar]
  15. OVARY Z., BENACERRAF B. IMMUNOLOGICAL SPECIFICITY OF THE SECONDARY RESPONSE WITH DINITROPHENYLATED PROTEINS. Proc Soc Exp Biol Med. 1963 Oct;114:72–76. doi: 10.3181/00379727-114-28589. [DOI] [PubMed] [Google Scholar]
  16. Paul W. E. Functional specificity of antigen-binding receptors of lymphocytes. Transplant Rev. 1970;5:130–166. doi: 10.1111/j.1600-065x.1970.tb00359.x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Raff M. C. Role of thymus-derived lymphocytes in the secondary humoral immune response in mice. Nature. 1970 Jun 27;226(5252):1257–1258. doi: 10.1038/2261257a0. [DOI] [PubMed] [Google Scholar]
  19. Rajewsky K., Schirrmacher V., Nase S., Jerne N. K. The requirement of more than one antigenic determinant for immunogenicity. J Exp Med. 1969 Jun 1;129(6):1131–1143. doi: 10.1084/jem.129.6.1131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Roelants G. E., Askonas B. A. Cell cooperation in antibody induction. The susceptibility of helper cells to specific lethal radioactive antigen. Eur J Immunol. 1971 Jun;1(3):151–157. doi: 10.1002/eji.1830010302. [DOI] [PubMed] [Google Scholar]
  21. Senyk G., Nitecki D., Goodman J. W. Immunogenicity of glucagon: determinants responsible for antibody binding and lymphocyte stimulation. Science. 1971 Jan 29;171(3969):407–408. doi: 10.1126/science.171.3969.407. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Wigzell H. Specific fractionation of immunocompetent cells. Transplant Rev. 1970;5:76–104. doi: 10.1111/j.1600-065x.1970.tb00357.x. [DOI] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES