Abstract
Previous studies have demonstrated that the B cells in immune and nonimmune mice manifest different major histocompatibility complex (MHC) collaborative phenotypes with antigen-specific T cells. Immune, or secondary B cells require syngeneic-like MHC recognition by collaborating T cells, and in its absence fail to be stimulated. Primary B cells manifest a much less stringent requisite for MHC recognition by T cells, and under conditions in which secondary B cells fail to be stimulated, primary B cells are stimulated to secrete IgM antibody. Experiments were conducted to determine whether the acquisition of the secondary B cells' MHC collaborative phenotype was dependent on the presence of T cells during in vivo immunization. B cell populations from T dependently and T independently immunized conventional BALB/c and athymic BALB/c nu/nu mice were compared in their ability to collaborate with allogeneic T cells. Although antigen alone promotes the differentiation of several secondary B cell characteristics, including an increase in the frequency of antigen- specific B cells and a preference for IgG1 antibody synthesis in vitro, the acquisition of the secondary B cells' MHC collaborative phenotype was dependent on the presence of T cells during in vivo immunization. B cell populations from T dependently and T independently immunized conventional BALB/c and athymic BALB/c nu/nu mice were compared in their ability to collaborate with allogeneic T cells. Although antigen alone promotes the differentiation of several secondary B cell characteristics, including an increase in the frequency of antigen- specific B cells and a preference of IgG1 antibody synthesis in vitro, the acquisition of the secondary B cells' MHC collaborative phenotype was found to be dependent on the presence of T cells during in vivo immunization. Thus, the restriction imposed on T cell-B-cell- collaborative interactions in secondary humoral immune responses appears to be the result of T dependent antigen-driven events.
Full Text
The Full Text of this article is available as a PDF (1.0 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Black S. J., van der Loo W., Loken M. R., Herzenberg L. A. Expression of IgD by murine lymphocytes. Loss of surface IgD indicates maturation of memory B cells. J Exp Med. 1978 Apr 1;147(4):984–996. doi: 10.1084/jem.147.4.984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bottomly K., Mosier D. E. Mice whose B cells cannot produce the T15 idiotype also lack an antigen-specific helper T cell required for T15 expression. J Exp Med. 1979 Dec 1;150(6):1399–1409. doi: 10.1084/jem.150.6.1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Braley-Mullen H. Secondary IgG responses to type 3 pneumococcal polysaccharide. III. T cell requirement for development of B memory cells. Eur J Immunol. 1977 Nov;7(11):775–781. doi: 10.1002/eji.1830071106. [DOI] [PubMed] [Google Scholar]
- Davie J. M., Paul W. E. Role of T lymphocytes in the humoral immune response. I. Proliferation of B lymphocytes in thymus-deprived mice. J Immunol. 1974 Nov;113(5):1438–1445. [PubMed] [Google Scholar]
- Elson C. O., Heck J. A., Strober W. T-cell regulation of murine IgA synthesis. J Exp Med. 1979 Mar 1;149(3):632–643. doi: 10.1084/jem.149.3.632. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorczynski R. M., Kennedy M. J., MacRae S., Steele E. J., Cunningham A. J. Restriction of antigen recognition in mouse B lymphocytes by genes mapping within the major histocompatibility complex. J Immunol. 1980 Feb;124(2):590–596. [PubMed] [Google Scholar]
- Herzenberg L. A., Black S. J., Tokuhisa T., Herzenberg L. A. Memory B cells at successive stages of differentiation. Affinity maturation and the role of IgD receptors. J Exp Med. 1980 May 1;151(5):1071–1087. doi: 10.1084/jem.151.5.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hetzelberger D., Eichmann K. Recognition of idiotypes in lymphocyte interactions. I. Idiotypic selectivity in the cooperation between T and B lymphocytes. Eur J Immunol. 1978 Dec;8(12):846–852. doi: 10.1002/eji.1830081205. [DOI] [PubMed] [Google Scholar]
- Kappler J. W., Marrack P. The role of H-2 linked genes in helper T-cell function. IV. Importance of T-cell genotype and host environment in I-region and Ir gene expression. J Exp Med. 1978 Dec 1;148(6):1510–1522. doi: 10.1084/jem.148.6.1510. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Katz D. H. Adaptive differentiation of murine lymphocytes. III. T and B lymphocytes display reciprocal preference for one another to develop optimal interacting partner cell sets. J Immunol. 1979 May;122(5):1937–1942. [PubMed] [Google Scholar]
- Katz D. H., Hamaoka T., Benacerraf B. Cell interactions between histoincompatible T and B lymphocytes. II. Failure of physiologic cooperative interactions between T and B lymphocytes from allogeneic donor strains in humoral response to hapten-protein conjugates. J Exp Med. 1973 Jun 1;137(6):1405–1418. doi: 10.1084/jem.137.6.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Loor F., Amstutz H., Hägg L. B., Mayor K. S., Roelants G. E. T lineage lymphocytes in nude mice born from homozygous nu/nu parents. Eur J Immunol. 1976 Sep;6(9):663–665. doi: 10.1002/eji.1830060914. [DOI] [PubMed] [Google Scholar]
- Mitchell G. F., Lafleur L., Andersson K. Evidence for readily induced tolerance to heterologous erythrocytes in nude mice. Scand J Immunol. 1974;3(1):39–49. doi: 10.1111/j.1365-3083.1974.tb01231.x. [DOI] [PubMed] [Google Scholar]
- Mongini P. K., Stein K. E., Paul W. E. T cell regulation of IgG subclass antibody production in response to T-independent antigens. J Exp Med. 1981 Jan 1;153(1):1–12. doi: 10.1084/jem.153.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nutt N., Haber J., Wortis H. H. Influence of Igh-linked gene products on the generation of T helper cells in the response to sheep erythrocytes. J Exp Med. 1981 May 1;153(5):1225–1235. doi: 10.1084/jem.153.5.1225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Okumura K., Julius M. H., Tsu T., Herzenberg L. A., Herzenberg L. A. Demonstration that IgG memory is carried by IgG-bearing cells. Eur J Immunol. 1976 Jul;6(7):467–472. doi: 10.1002/eji.1830060704. [DOI] [PubMed] [Google Scholar]
- Pierce S. K., Klinman N. R. Allogeneic carrier-specific enhancement of hapten-specific secondary B-cell responses. J Exp Med. 1976 Nov 2;144(5):1254–1262. doi: 10.1084/jem.144.5.1254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pierce S. K., Klinman N. R. Antibody-specific immunoregulation. J Exp Med. 1977 Aug 1;146(2):509–519. doi: 10.1084/jem.146.2.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pierce S. K., Klinman N. R., Maurer P. H., Merryman C. F. Role of the major histocompatibility gene products in regulating the antibody response to dinitrophenylated poly(L-Glu55,L-Ala35,L-Phe9)n. J Exp Med. 1980 Aug 1;152(2):336–349. doi: 10.1084/jem.152.2.336. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pierce S. K., Klinman N. R. Multiple B cell stimulation by individual antigen-specific T lymphocytes. Eur J Immunol. 1981 Feb;11(2):71–75. doi: 10.1002/eji.1830110202. [DOI] [PubMed] [Google Scholar]
- Press J. L., Klinman N. R. Frequency of hapten-specific B cells in neonatal and adult murine spleens. Eur J Immunol. 1974 Mar;4(3):155–159. doi: 10.1002/eji.1830040302. [DOI] [PubMed] [Google Scholar]
- Schrader J. W. The role of T cells in IgG production; thymus-dependent antigens induce B cell memory in the absence of T cells. J Immunol. 1975 Jun;114(6):1665–1669. [PubMed] [Google Scholar]
- Schwartz R. H., Yano A., Paul W. E. Interaction between antigen-presenting cells and primed T lymphocytes: an assessment of Ir gene expression in the antigen-presenting cell. Immunol Rev. 1978;40:153–180. doi: 10.1111/j.1600-065x.1978.tb00405.x. [DOI] [PubMed] [Google Scholar]
- Singer A., Hathcock K. S., Hodes R. J. Self recognition in allogeneic radiation bone marrow chimeras. A radiation-resistant host element dictates the self specificity and immune response gene phenotype of T-helper cells. J Exp Med. 1981 May 1;153(5):1286–1301. doi: 10.1084/jem.153.5.1286. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Speck N. A., Maurer P. H., Pierce S. K. The functional helper T cell repertoire specific for L-glutamic acid60-L-alanine30-L-tyrosine10 (GAT). J Immunol. 1981 Nov;127(5):1772–1777. [PubMed] [Google Scholar]
- Stockinger H., Bartlett R., Pfizenmaier K., Röllinghoff M., Wagner H. H-2 restriction as a consequence of intentional priming. Frequency analysis of alloantigen-restricted, trinitrophenyl-specific cytotoxic T lymphocyte precursors within thymocytes of normal mice. J Exp Med. 1981 Jun 1;153(6):1629–1639. doi: 10.1084/jem.153.6.1629. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stockinger H., Pfizenmaier K., Hardt C., Rodt H., Röllinghoff M., Wagner H. H-2 restriction as a consequence of intentional priming: T cells of fully allogeneic chimeric mice as well as of normal mice respond to foreign antigens in the context of H-2 determinants not encountered on thymic epithelial cells. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7390–7394. doi: 10.1073/pnas.77.12.7390. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas D. W., Shevach E. M. Nature of the antigenic complex recognized by T lymphocytes: specific sensitization by antigens associated with allogeneic macrophages. Proc Natl Acad Sci U S A. 1977 May;74(5):2104–2108. doi: 10.1073/pnas.74.5.2104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson D. B., Lindahl K. F., Wilson D. H., Sprent J. The generation of killer cells to trinitrophenyl-modified allogeneic targets by lymphocyte populations negatively selected to strong alloantigens. J Exp Med. 1977 Aug 1;146(2):361–367. doi: 10.1084/jem.146.2.361. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woodland R., Cantor H. Idiotype-specific T helper cells are required to induce idiotype-positive B memory cells to secrete antibody. Eur J Immunol. 1978 Aug;8(8):600–606. doi: 10.1002/eji.1830080812. [DOI] [PubMed] [Google Scholar]
- 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]