Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1970 Nov 30;132(6):1122–1137. doi: 10.1084/jem.132.6.1122

ANTIGEN-SPECIFIC CELLS IN MOUSE BONE MARROW

I. LASTING EFFECTS OF PRIMING ON IMMUNOCYTE PRODUCTION BY TRANSFERRED MARROW

Harold C Miller 1, Gustavo Cudkowicz 1
PMCID: PMC2180502  PMID: 4101972

Abstract

Graded numbers of marrow cells and 5 x 107 thymocytes were mixed in vitro and transplanted into X-irradiated (C3H x C57BL/10)F1 mice. Upon injection of sheep or chicken erythrocytes, splenic plaque-forming cells secreting IgM (direct PFC) or IgG (indirect PFC) hemolytic antibody were enumerated at the time of peak responses. Anti-sheep and anti-chicken primary PFC responses elicited by nonimmune marrow cells differed sharply from each other under the conditions of limiting dilution assays. The frequencies of anti-chicken responses in recipients of different numbers of marrow cells conformed to the predictions of the Poisson model, while the frequencies of anti-sheep responses did not. Hence, the function of certain marrow-derived cells was expressed differentially during the two immune responses, to exclude that the same precursor units generated anti-sheep or anti-chicken PFC. The former precursor cells or units were functionally more heterogeneous than the latter. Immunization of marrow donors against sheep erythrocytes did not alter the population of cells engaged in anti-chicken responses, since limiting dilution assays with immune and nonimmune marrow cells gave identical results. However, anti-sheep immunization altered specifically the cell population engaged in anti-sheep responses, in two ways: (a) potentially immunocompetent marrow cells underwent antigen-dependent differentiation or maturation, to become functionally homogeneous. Consequently, the frequencies of PFC responses in limiting dilution assays conformed to the Poisson model; the changes occurred independently in class-restricted precursors of direct and indirect PFC. (b) marrow cells capable of inhibiting precursors of direct anti-sheep PFC arose in primed mice. The inhibition, which was specific, could have been effected directly by marrow cells or by a diffusable product such as IgG antibody. Results indicated that potentially immunocompetent cells of mouse marrow with distinct functions were antigen specific and antigen sensitive.

Full Text

The Full Text of this article is available as a PDF (935.0 KB).

Selected References

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

  1. Armstrong W. D., Diener E., Shellam G. R. Antigen-reactive cells in normal, immunized, and tolerant mice. J Exp Med. 1969 Feb 1;129(2):393–410. doi: 10.1084/jem.129.2.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Claman H. N., Chaperon E. A., Triplett R. F. Immunocompetence of transferred thymus-marrow cell combinations. J Immunol. 1966 Dec;97(6):828–832. [PubMed] [Google Scholar]
  5. Cudkowicz G., Shearer G. M., Ito T. Cellular differentiation of the immune system of mice. VI. Strain differences in class differentiation and other properties of marrow cells. J Exp Med. 1970 Oct 1;132(4):623–635. doi: 10.1084/jem.132.4.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cudkowicz G., Shearer G. M., Priore R. L. Cellular differentiation of the immune system of mice. V. Class differentiation in marrow precursors of plaque-forming cells. J Exp Med. 1969 Sep 1;130(3):481–491. doi: 10.1084/jem.130.3.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gershon R. K., Wallis V., Davies A. J., Leuchars E. Inactivation of thymus cells after multiple injections of antigen. Nature. 1968 Apr 27;218(5139):380–381. doi: 10.1038/218380a0. [DOI] [PubMed] [Google Scholar]
  8. Haughton G., Adams D. O. Specific immunosuppression by minute doses of passive antibody. II. The site of action. J Reticuloendothel Soc. 1970 Apr;7(4):500–517. [PubMed] [Google Scholar]
  9. Henry C., Jerne N. K. Competition of 19S and 7S antigen receptors in the regulation of the primary immune response. J Exp Med. 1968 Jul 1;128(1):133–152. doi: 10.1084/jem.128.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kennedy J. C., Treadwell P. E., Lennox E. S. Antigen-specific synergism in the immune response of irradiated mice given marrow cells and peritoneal cavity cells or extracts. J Exp Med. 1970 Aug 1;132(2):353–367. doi: 10.1084/jem.132.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Mitchell G. F., Miller J. F. Cell to cell interaction in the immune response. II. The source of hemolysin-forming cells in irradiated mice given bone marrow and thymus or thoracic duct lymphocytes. J Exp Med. 1968 Oct 1;128(4):821–837. doi: 10.1084/jem.128.4.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Mosier D. E., Fitch F. W., Rowley D. A., Davies A. J. Cellular deficit in thymectomized mice. Nature. 1970 Jan 17;225(5229):276–277. doi: 10.1038/225276a0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Pierce C. W. Immune responses in vitro. I. Cellular requirements for the immune response by nonprimed and primed spleen cells in vitro. J Exp Med. 1969 Aug 1;130(2):345–364. doi: 10.1084/jem.130.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Playfair J. H. Strain differences in the immune response of mice. II. Responses by neonatal cells in irradiated adult hosts. Immunology. 1968 Dec;15(6):815–826. [PMC free article] [PubMed] [Google Scholar]
  19. Plotz P. H., Talal N., Asofsky R. Assignment of direct and facilitated hemolytic plaques in mice to specific immunoglobulin classes. J Immunol. 1968 Apr;100(4):744–751. [PubMed] [Google Scholar]
  20. Shearer G. M., Cudkowicz G. Cellular differentiation of the immune system of mice. 3. Separate antigen-sensitive units for different types of anti-sheep immunocytes formed by marrow-thymus cell mixtures. J Exp Med. 1969 May 1;129(5):935–951. doi: 10.1084/jem.129.5.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shearer G. M., Cudkowicz G., Connell M. S., Priore R. L. Cellular differentiation of the immune system of mice. I. Separate splenic antigen-sensitive units for different types of anti-sheep antibody-forming cells. J Exp Med. 1968 Sep 1;128(3):437–457. doi: 10.1084/jem.128.3.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Shearer G. M., Cudkowicz G., Priore R. L. Cellular differentiation of the immune system of mice. II. Frequency of unipotent splenic antigen-sensitive units after immunization with sheep erythrocytes. J Exp Med. 1969 Jan 1;129(1):185–199. doi: 10.1084/jem.129.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shortman K., Diener E., Russell P., Armstrong W. D. The role of nonlymphoid accessory cells in the immune response to different antigens. J Exp Med. 1970 Mar 1;131(3):461–482. doi: 10.1084/jem.131.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shortman K., Diener E., Russell P., Armstrong W. D. The role of nonlymphoid accessory cells in the immune response to different antigens. J Exp Med. 1970 Mar 1;131(3):461–482. doi: 10.1084/jem.131.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Wortis H. H., Taylor R. B., Dresser D. W. Antibody production studied by means of the LHG assay. I. The splenic response of CBA mice to sheep erythrocytes. Immunology. 1966 Dec;11(6):603–616. [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES