Skip to main content
NCBI home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1972 Jan 31;135(2):165–184. doi: 10.1084/jem.135.2.165

IMMUNOLOGICAL MEMORY IN MICE

III. MEMORY TO HETEROLOGOUS ERYTHROCYTES IN BOTH T CELL AND B CELL POPULATIONS AND REQUIREMENT FOR T CELLS IN EXPRESSION OF B CELL MEMORY. EVIDENCE USING IMMUNOGLOBULIN ALLOTYPE AND MOUSE ALLOANTIGEN THETA MARKERS WITH CONGENIC MICE

G F Mitchell 1, Eva L Chan 1, Marion S Noble 1, I L Weissman 1, R I Mishell 1, L A Herzenberg 1
PMCID: PMC2180523  PMID: 4110524

Abstract

Using anti-allotype sera and AKR anti θC3H sera, a requirement for two cell types has been demonstrated in the adoptive secondary response of mice to heterologous erythrocytes. The cell types have been designated B cells [precursors of plaque-forming cells (PFC)] and T cells (thymus-influenced cells, not providing precursors of detectable PFC). The in vivo indirect PFC response of spleen cells from primed mice is markedly reduced by in vitro treatment of the cells with a mixture of anti-θ serum and guinea pig serum (Anti θ + GPS). This B cell response is fully restored to control levels by thymus cells from normal mice which do not themselves provide precursors of indirect PFC. Thus memory is carried by the B cell lineage but the expression of this memory is dependent on the presence of a cell population which is sensitive to Anti θ + GPS and which is replaced functionally by unprimed T cells. When assayed for T cell activity, thoracic duct cells from specifically primed mice are better than cells from nonspecifically primed mice in restoring the B cell response of spleen cells from immunized mice. Moreover, the T cell activity of a reconstitutive cell population from primed mice is reduced by incubation with Anti θ + GPS. We conclude that memory to heterologous erythrocyte antigens is carried by the T cell lineage as well as the B cell lineage even though unprimed T cells are sufficient for expression of B cell memory.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Aoki T., Hämmerling U., De Harven E., Boyse E. A., Old L. J. Antigenic structure of cell surfaces. An immunoferritin study of the occurrence and topography of H-2' theta, and TL alloantigens on mouse cells. J Exp Med. 1969 Nov 1;130(5):979–1001. doi: 10.1084/jem.130.5.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BOAK J. L., WOODRUFF M. F. A MODIFIED TECHNIQUE FOR COLLECTING MOUSE THORACIC DUCT LYMPH. Nature. 1965 Jan 23;205:396–397. doi: 10.1038/205396a0. [DOI] [PubMed] [Google Scholar]
  3. Boyse E. A., Miyazawa M., Aoki T., Old L. J. Ly-A and Ly-B: two systems of lymphocyte isoantigens in the mouse. Proc R Soc Lond B Biol Sci. 1968 Jun 11;170(1019):175–193. doi: 10.1098/rspb.1968.0032. [DOI] [PubMed] [Google Scholar]
  4. Chan E. L., Mishell R. I., Mitchell G. F. Cell interaction in an immune response in vitro: requirement for theta-carrying cells. Science. 1970 Dec 11;170(3963):1215–1217. doi: 10.1126/science.170.3963.1215. [DOI] [PubMed] [Google Scholar]
  5. Chiller J. M., Habicht G. S., Weigle W. O. Cellular sites of immunologic unresponsiveness. Proc Natl Acad Sci U S A. 1970 Mar;65(3):551–556. doi: 10.1073/pnas.65.3.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chiller J. M., Habicht G. S., Weigle W. O. Kinetic differences in unresponsiveness of thymus and bone marrow cells. Science. 1971 Feb 26;171(3973):813–815. doi: 10.1126/science.171.3973.813. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Cohen M. W., Jacobson E. B., Thorbecke G. J. Gamma-globulin and antibody formation in vitro. V. The secondary response made by splenic white and red pulp with reference to the role of secondary nodules. J Immunol. 1966 Jun;96(6):944–952. [PubMed] [Google Scholar]
  9. Cunningham A. J. Studies on the cellular basis of IgM immunological memory. The induction of antibody formation in bone marrow cells by primed spleen cells. Immunology. 1969 Dec;17(6):933–942. [PMC free article] [PubMed] [Google Scholar]
  10. Cunningham A. J. Studies on the cellular basis of IgM immunological memory. Immunology. 1969 May;16(5):621–632. [PMC free article] [PubMed] [Google Scholar]
  11. Davies A. J. The thymus and the cellular basis of immunity. Transplant Rev. 1969;1:43–91. doi: 10.1111/j.1600-065x.1969.tb00136.x. [DOI] [PubMed] [Google Scholar]
  12. Goodman J. W., Shinpock S. G. Influence of thymus cells on erythropoiesis of parental marrow in irradiated hybrid mice. Proc Soc Exp Biol Med. 1968 Nov;129(2):417–422. doi: 10.3181/00379727-129-33334. [DOI] [PubMed] [Google Scholar]
  13. Hege J. S., Cole L. J. Antibody plaque-forming cells: kinetics of primary and secondary responses. J Immunol. 1966 Apr;96(4):559–569. [PubMed] [Google Scholar]
  14. Jacobson E. B., L'age-Stehr J., Herzenberg L. A. Immunological memory in mice. II. Cell interactions in the secondary immune response studies by means of immunoglobulin allotype markers. J Exp Med. 1970 Jun 1;131(6):1109–1120. doi: 10.1084/jem.131.6.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Klein J., Herzenberg L. A. Congenic mouse strains with different immunoglobulin allotypes. I. Breeding scheme, histocompatibility tests, and kinetics of gamma G2a-globulin production by transferred cells for C3H.SW and its congenic partner CWB/5. Transplantation. 1967 Nov;5(6):1484–1495. doi: 10.1097/00007890-196711000-00013. [DOI] [PubMed] [Google Scholar]
  16. L'age-Stehr J., Herzenberg L. A. Immunological memory in mice. I. Physical separation and partial characterization of memory cells for different immunoglobulin classes from each other and from antibody-producing cells. J Exp Med. 1970 Jun 1;131(6):1093–1108. doi: 10.1084/jem.131.6.1093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Many A., Schwartz R. S. Drug-induced immunologic tolerance: site of action of cyclophosphamide. Proc Soc Exp Biol Med. 1970 Mar;133(3):754–757. doi: 10.3181/00379727-133-34558. [DOI] [PubMed] [Google Scholar]
  18. Miller J. F., Dukor P., Grant G., Sinclair N. R., Sacquet E. The immunological responsiveness of germ-free mice thymectomized at birth. I. Antibody production and skin homograft rejection. Clin Exp Immunol. 1967 Sep;2(5):531–542. [PMC free article] [PubMed] [Google Scholar]
  19. Miller J. F., Mitchell G. F. Cell to cell interaction in the immune response. V. Target cells for tolerance induction. J Exp Med. 1970 Apr 1;131(4):675–699. doi: 10.1084/jem.131.4.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Mishell R. I., Dutton R. W. Immunization of dissociated spleen cell cultures from normal mice. J Exp Med. 1967 Sep 1;126(3):423–442. doi: 10.1084/jem.126.3.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mitchell G. F., Miller J. F. Immunological activity of thymus and thoracic-duct lymphocytes. Proc Natl Acad Sci U S A. 1968 Jan;59(1):296–303. doi: 10.1073/pnas.59.1.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nettesheim P., Williams M. L. Regenerative potential of immunocompetent cells. II. Factors influencing recovery of secondary antibody-forming potential from x-irradiation. J Immunol. 1968 Apr;100(4):760–770. [PubMed] [Google Scholar]
  24. Nossal G. J., Cunningham A., Mitchell G. F., Miller J. F. Cell to cell interaction in the immune response. 3. Chromosomal marker analysis of single antibody-forming cells in reconstituted, irradiated, or thymectomized mice. J Exp Med. 1968 Oct 1;128(4):839–853. doi: 10.1084/jem.128.4.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Raff M. C. Two distinct populations of peripheral lymphocytes in mice distinguishable by immunofluorescence. Immunology. 1970 Oct;19(4):637–650. [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Schimpl A., Wecker E. Inhibition of in vitro immune response by treatment of spleen cell suspensions with anti-theta serum. Nature. 1970 Jun 27;226(5252):1258–1259. doi: 10.1038/2261258a0. [DOI] [PubMed] [Google Scholar]
  30. Schlesinger M., Yron I. Serologic demonstration of a thymus-dependent population of lymph-node cells. J Immunol. 1970 Apr;104(4):798–804. [PubMed] [Google Scholar]
  31. Sercarz E. E., Byers V. S. The X-Y-Z scheme of immunocyte maturation. 3. Early IgM memory and the nature of the memory cell. J Immunol. 1967 Apr;98(4):836–843. [PubMed] [Google Scholar]
  32. Shearer G. M., Cudkowicz G. Distinct events in the immune response elicited by transferred marrow and thymus cells. I. Antigen requirements and priferation of thymic antigen-reactive cells. J Exp Med. 1969 Dec 1;130(6):1243–1261. doi: 10.1084/jem.130.6.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. TILL J. E., McCULLOCH E. A. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res. 1961 Feb;14:213–222. [PubMed] [Google Scholar]
  34. Takahashi T., Carswell E. A., Thorbecke G. J. Surface antigens of immunocompetent cells. I. Effect of theta and PC.1 alloantisera on the ability of spleen cells to transfer immune responses. J Exp Med. 1970 Dec 1;132(6):1181–1190. doi: 10.1084/jem.132.6.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. Wu A. M., Till J. E., Siminovitch L., McCulloch E. A. Cytological evidence for a relationship between normal hemotopoietic colony-forming cells and cells of the lymphoid system. J Exp Med. 1968 Mar 1;127(3):455–464. doi: 10.1084/jem.127.3.455. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES