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. 1983 Aug 1;158(2):265–279. doi: 10.1084/jem.158.2.265

Subpopulations of B cells distinguished by cell surface expression of Ia antigens. Correlation of Ia and idiotype during activation by cloned Ia-restricted T cells

PMCID: PMC2187353  PMID: 6193216

Abstract

We have investigated in vitro the induction of antibody responses to phosphorylcholine (PC) by cloned T helper (Th) cell lines. The cloned Th cells are antigen specific, in this case ovalbumin (OVA), self-Ia recognizing, and induce antibody secretion only if the hapten, PC, is physically linked to the carrier (OVA) molecule. The plaque-forming cell (PFC) response generated in the presence of cloned Th cells is idiotypically diverse with 5-40% of the secreting B cells bearing the TEPC-15 (T15) idiotype. The interaction of the cloned Th cells and unprimed B cells requires recognition of B cell surface Ia glycoproteins for all B cells activated to secrete anti-PC antibody, whether they be T15-bearing or not. More importantly, however, effective interaction between a cloned Th cell and a B cell is determined by the quantity of B cell surface Ia glycoproteins. Our results indicate that quantitative differences in B cell surface Ia antigens are directly related to B cell activation by the cloned Th cell. The high Ia density B cells are most easily activated by cloned Th cells, and these appear to be mainly non-T15-bearing. These data suggest that the failure of cloned Th cells to effectively activate T15- bearing B cells in vitro may be due to the lower relative Ia density of these B cells and therefore to their inability to interact effectively with cloned Ia-recognizing Th cells. These results imply that monoclonal T cells may distinguish between T15-bearing and non-T15- bearing B cells based on their Ia density.

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Selected References

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  1. Benacerraf B., Germain R. N. The immune response genes of the major histocompatibility complex. Immunol Rev. 1978;38:70–119. doi: 10.1111/j.1600-065x.1978.tb00385.x. [DOI] [PubMed] [Google Scholar]
  2. Bottomly K., Mathieson B. J., Mosier D. E. Anti-idiotype induced regulation of helper cell function for the response to phosphorylcholine in adult BALB/c mice. J Exp Med. 1978 Nov 1;148(5):1216–1227. doi: 10.1084/jem.148.5.1216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Cerny J., Caulfield M. J. Stimulation of specific antibody-forming cells in antigen-primed nude mice by the adoptive transfer of syngeneic anti-idiotypic T cells. J Immunol. 1981 Jun;126(6):2262–2266. [PubMed] [Google Scholar]
  5. Claflin J. L., Cubberley M. Clonal nature of the immune response to phosphocholine. VI. Molecular uniformity of a single idiotype among BALB/c mice. J Immunol. 1978 Oct;121(4):1410–1415. [PubMed] [Google Scholar]
  6. Cosenza H., Julius M. H., Augustin A. A. Idiotypes as variable region markers: analogies between receptors on phosphorylcholine-specific T and B lymphocytes. Immunol Rev. 1977;34:3–33. doi: 10.1111/j.1600-065x.1977.tb00366.x. [DOI] [PubMed] [Google Scholar]
  7. Cowing C., Schwartz B. D., Dickler H. B. Macrophage Ia antigens. I. macrophage populations differ in their expression of Ia antigens. J Immunol. 1978 Feb;120(2):378–384. [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. Heterogeneity of the BALB/c antiphosphorylcholine antibody response at the precursor cell level. J Exp Med. 1975 Jan 1;141(1):56–71. doi: 10.1084/jem.141.1.56. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Greenstein J. L., Lord E. M., Horan P., Kappler J. W., Marrack P. Functional subsets of B cells defined by quantitative differences in surface I-A. J Immunol. 1981 Jun;126(6):2419–2423. [PubMed] [Google Scholar]
  11. Henry C., Chan E. L., Kodlin D. Expression and function of I region products on immunocompetent cells. II. I region products in T-B interaction. J Immunol. 1977 Aug;119(2):744–748. [PubMed] [Google Scholar]
  12. Huber B. T. Antigenic marker on a functional subpopulation of B cells, controlled by the I-A subregion of the H-2 complex. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3460–3463. doi: 10.1073/pnas.76.7.3460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Janeway C. A., Jr, Bottomly K., Jones B., Jones P. P., Lerner E. A., Matis L. A., McNicholas J. M., Murphy D. B., Schwartz R. H. Helper T cells specific for protein antigens: role of self major histocompatibility complex and immunoglobulin gene products. Adv Exp Med Biol. 1982;150:53–71. doi: 10.1007/978-1-4684-4331-8_4. [DOI] [PubMed] [Google Scholar]
  14. Jones B., Janeway C. A., Jr Cooperative interaction of B lymphocytes with antigen-specific helper T lymphocytes is MHC restricted. Nature. 1981 Aug 6;292(5823):547–549. doi: 10.1038/292547a0. [DOI] [PubMed] [Google Scholar]
  15. Julius M. H., Chiller J. M., Sidman C. L. Major histocompatibility complex-restricted cellular interactions determining B cell activation. Eur J Immunol. 1982 Aug;12(8):627–633. doi: 10.1002/eji.1830120802. [DOI] [PubMed] [Google Scholar]
  16. Kappler J. W., Skidmore B., White J., Marrack P. Antigen-inducible, H-2-restricted, interleukin-2-producing T cell hybridomas. Lack of independent antigen and H-2 recognition. J Exp Med. 1981 May 1;153(5):1198–1214. doi: 10.1084/jem.153.5.1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kenny J. J., Guelde G., Claflin J. L., Scher I. Altered idiotype response to phosphocholine in mice bearing an x-linked immune defect. J Immunol. 1981 Oct;127(4):1629–1633. [PubMed] [Google Scholar]
  18. Lerner E. A., Matis L. A., Janeway C. A., Jr, Jones P. P., Schwartz R. H., Murphy D. B. Monoclonal antibody against an Ir gene product? J Exp Med. 1980 Oct 1;152(4):1085–1101. doi: 10.1084/jem.152.4.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Matis L. A., Jones P. P., Murphy D. B., Hedrick S. M., Lerner E. A., Janeway C. A., Jr, McNicholas J. M., Schwartz R. H. Immune response gene function correlates with the expression of an Ia antigen. II. A quantitative deficiency in Ae:E alpha complex expression causes a corresponding defect in antigen-presenting cell function. J Exp Med. 1982 Feb 1;155(2):508–523. doi: 10.1084/jem.155.2.508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Melchers F., Andersson J., Lernhardt W., Schreier M. H. H-2-unrestricted polyclonal maturation without replication of small B cells induced by antigen-activated T cell help factors. Eur J Immunol. 1980 Sep;10(9):679–685. doi: 10.1002/eji.1830100905. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Mond J. J., Kessler S., Finkelman F. D., Paul W. E., Scher I. Heterogeneity of Ia expression on normal B cells, neonatal B cells, and on cells from B cell-defective CBA/N mice. J Immunol. 1980 Apr;124(4):1675–1682. [PubMed] [Google Scholar]
  23. Mond J. J., Lieberman R., Inman J. K., Mosier D. E., Paul W. E. Inability of mice with a defect in B-lymphocyte maturation to respond to phosphorycholine on immunogenic carriers. J Exp Med. 1977 Oct 1;146(4):1138–1142. doi: 10.1084/jem.146.4.1138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mond J. J., Seghal E., Kung J., Finkelman F. D. Increased expression of I-region-associated antigen (Ia) on B cells after cross-linking of surface immunoglobulin. J Immunol. 1981 Sep;127(3):881–888. [PubMed] [Google Scholar]
  25. Press J. L., Strober S., Klinman N. R. Characterization of B cell subpopulations by velocity sedimentation, surface ia antigens and immune function. Eur J Immunol. 1977 Jun;7(6):329–335. doi: 10.1002/eji.1830070602. [DOI] [PubMed] [Google Scholar]
  26. Ratcliffe M. J., Julius M. H. H-2-restricted T-B cell interactions involved in polyspecific B cell responses mediated by soluble antigen. Eur J Immunol. 1982 Aug;12(8):634–641. doi: 10.1002/eji.1830120803. [DOI] [PubMed] [Google Scholar]
  27. Rosenthal A. S., Shevach E. M. Function of macrophages in antigen recognition by guinea pig T lymphocytes. I. Requirement for histocompatible macrophages and lymphocytes. J Exp Med. 1973 Nov 1;138(5):1194–1212. doi: 10.1084/jem.138.5.1194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sachs D. H., Cone J. L. A mouse B-cell alloantigen determined by gene(s) linked to the major histocompatibility complex. J Exp Med. 1973 Dec 1;138(6):1289–1304. doi: 10.1084/jem.138.6.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Sieckmann D. G. The use of anti-immunoglobulins to induce a signal for cell division in B lymphocytes via their membrane IgM and IgD. Immunol Rev. 1980;52:181–210. doi: 10.1111/j.1600-065x.1980.tb00335.x. [DOI] [PubMed] [Google Scholar]
  31. Singer A., Asano Y., Shigeta M., Hathcock K. S., Ahmed A., Fathman C. G., Hodes R. J. Distinct B cell subpopulations differ in their genetic requirements for activation by T helper cells. Immunol Rev. 1982;64:137–160. doi: 10.1111/j.1600-065x.1982.tb00422.x. [DOI] [PubMed] [Google Scholar]
  32. Singer A., Morrissey P. J., Hathcock K. S., Ahmed A., Scher I., Hodes R. J. Role of the major histocompatibility complex in T cell activation of B cell subpopulations Lyb-5+ and Lyb-5- B cell subpopulations differ in their requirement for major histocompatibility complex-restricted T cell recognition. J Exp Med. 1981 Aug 1;154(2):501–516. doi: 10.1084/jem.154.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sprent J. Restricted helper function of F1 hybrid T cells positively selected to heterologous erythrocytes in irradiated parental strain mice. II. Evidence for restrictions affecting helper cell induction and T-B collaboration, both mapping to the K-end of the H-2 complex. J Exp Med. 1978 Apr 1;147(4):1159–1174. doi: 10.1084/jem.147.4.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sprent J. Restricted helper function of F1 leads to parent bone marrow chimeras controlled by K-end of H-2 complex. J Exp Med. 1978 Jun 1;147(6):1838–1842. doi: 10.1084/jem.147.6.1838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sredni B., Tse H. Y., Chen C., Schwartz R. H. Antigen-specific clones of proliferating T lymphocytes. I. Methodology, specificity, and MHC restriction. J Immunol. 1981 Jan;126(1):341–347. [PubMed] [Google Scholar]

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