Abstract
The IgM antibody response to Type III pneumococcal polysaccharide (SSS-III) was assessed in F1, F2, and backcross progeny derived from high (BALB/cAnN) and extremely low (CBA/HN) responding parental strains of inbred mice. The results of these studies indicated that a major component involved in the antibody response is X-linked, i.e., carried on the X chromosome; this component determines responsiveness to SSS-III in an almost quantal or "all-or-none" manner. Other factors, presumably autosomal genes, regulate the magnitude of the antibody response produced by mice possessing the X-linked gene; these appear to influence independently the number of antibody-producing cells found after immunization and the amount of antibody made by such cells. Strains of inbred mice varied widely in their ability to respond to SSS-III. Responsiveness was not associated with H-2 histocompatibility type. The implications of these findings with respect to the genetic control of the antibody response to SSS-III are discussed.
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- ALDRICH R. A., STEINBERG A. G., CAMPBELL D. C. Pedigree demonstrating a sex-linked recessive condition characterized by draining ears, eczematoid dermatitis and bloody diarrhea. Pediatrics. 1954 Feb;13(2):133–139. [PubMed] [Google Scholar]
- Allison A. C., Denman A. M., Barnes R. D. Cooperating and controlling functions of thymus-derived lymphocytes in relation to autoimmunity. Lancet. 1971 Jul 17;2(7716):135–140. doi: 10.1016/s0140-6736(71)92306-3. [DOI] [PubMed] [Google Scholar]
- BRUTON O. C. Agammaglobulinemia. Pediatrics. 1952 Jun;9(6):722–728. [PubMed] [Google Scholar]
- Baker P. H., Stashak P. W. Quantitative and qualitative studies on the primary antibody response to pneumococcal polysaccharides at ehe cellular level. J Immunol. 1969 Dec;103(6):1342–1348. [PubMed] [Google Scholar]
- Baker P. J., Barth R. F., Stashak P. W., Amsbaugh D. F. Enhancement of the antibody response to type 3 pneumococcal polysaccharide in mice treated with antilymphocyte serum. J Immunol. 1970 May;104(5):1313–1315. [PubMed] [Google Scholar]
- Baker P. J., Prescott B., Stashak P. W., Amsbaugh D. F. Characterization of the antibody response to type 3 pneumococcal polysaccharide at the cellular level. 3. Studies on the average avidity of the antibody produced by specific plaque-forming cells. J Immunol. 1971 Sep;107(3):719–724. [PubMed] [Google Scholar]
- Baker P. J., Stashak P. W., Amsbaugh D. F., Prescott B., Barth R. F. Evidence for the existence of two functionally distinct types of cells which regulate the antibody response to type 3 pneumococcal polysaccharide. J Immunol. 1970 Dec;105(6):1581–1583. [PubMed] [Google Scholar]
- Baker P. J., Stashak P. W., Amsbaugh D. F., Prescott B. Characterization of the antibody response to type 3 pneumococcal polysaccharide at the cellular level. I. Dose-response studies and the effect of prior immunization on the magnitude of the antibody response. Immunology. 1971 Apr;20(4):469–480. [PMC free article] [PubMed] [Google Scholar]
- Baker P. J., Stashak P. W., Amsbaugh D. F., Prescott B. Characterization of the antibody response to type 3 pneumococcal polysaccharide at the cellular level. II. Studies on the relative rate of antibody synthesis and release by antibody-producing cells. Immunology. 1971 Apr;20(4):481–492. [PMC free article] [PubMed] [Google Scholar]
- Baker P. J., Stashak P. W., Prescott B. Use of erythrocytes sensitized with purified pneumococcal polysaccharides for the assay of antibody and antibody-producing cells. Appl Microbiol. 1969 Mar;17(3):422–426. doi: 10.1128/am.17.3.422-426.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benacerraf B., McDevitt H. O. Histocompatibility-linked immune response genes. Science. 1972 Jan 21;175(4019):273–279. doi: 10.1126/science.175.4019.273. [DOI] [PubMed] [Google Scholar]
- Braley H. C., Freeman M. J. Strain differences in the antibody plaque-forming cell responses of inbred mice to pneumococcal polysaccharide. Cell Immunol. 1971 Feb;2(1):73–81. doi: 10.1016/0008-8749(71)90026-8. [DOI] [PubMed] [Google Scholar]
- 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]
- Cooper M. D., Chae H. P., Lowman J. T., Krivit W., Good R. A. Wiskott-Aldrich syndrome. An immunologic deficiency disease involving the afferent limb of immunity. Am J Med. 1968 Apr;44(4):499–513. doi: 10.1016/0002-9343(68)90051-x. [DOI] [PubMed] [Google Scholar]
- Davies A. J., Carter R. L., Leuchars E., Wallis V., Dietrich F. M. The morphology of immune reactions in normal, thymectomized and reconstituted mice. 3. Response to bacterial antigens: salmonellar flagellar antigen and pneumococcal plysaccharide. Immunology. 1970 Dec;19(6):945–957. [PMC free article] [PubMed] [Google Scholar]
- Droege W. Amplifying and suppressive effect of thymus cells. Nature. 1971 Dec 31;234(5331):549–551. doi: 10.1038/234549a0. [DOI] [PubMed] [Google Scholar]
- GITLIN D., CRAIG J. M. THE THYMUS AND OTHER LYMPHOID TISSUES IN CONGENITAL AGAMMAGLOBULINEMIA. I. THYMIC ALYMPHOPLASIA AND LYMPHOCYTIC HYPOPLASIA AND THEIR RELATION TO INFECTION. Pediatrics. 1963 Oct;32:517–530. [PubMed] [Google Scholar]
- Gershon R. K., Cohen P., Hencin R., Liebhaber S. A. Suppressor T cells. J Immunol. 1972 Mar;108(3):586–590. [PubMed] [Google Scholar]
- Gershon R. K., Kondo K. Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology. 1970 May;18(5):723–737. [PMC free article] [PubMed] [Google Scholar]
- Gershon R. K., Kondo K. Infectious immunological tolerance. Immunology. 1971 Dec;21(6):903–914. [PMC free article] [PubMed] [Google Scholar]
- Grundbacher F. J. Human X chromosome carries quantitative genes for immunoglobulin M. Science. 1972 Apr 21;176(4032):311–312. doi: 10.1126/science.176.4032.311. [DOI] [PubMed] [Google Scholar]
- HUMPHREY J. H., PARROTT D. M., EAST J. STUDIES ON GLOBULIN AND ANTIBODY PRODUCTION IN MICE THYMECTOMIZED AT BIRTH. Immunology. 1964 Jul;7:419–439. [PMC free article] [PubMed] [Google Scholar]
- Horiuchi A., Waksman B. H. Role of the thymus in tolerance. 8. Relative effectiveness of nonaggregated and heat-aggregated bovine gamma globulin, injected directly into lymphoid organs of normal rats, in suppressing immune responsiveness. J Immunol. 1968 Dec;101(6):1322–1332. [PubMed] [Google Scholar]
- Howard J. G., Christie G. H., Courtenay B. M., Leuchars E., Davies A. J. Studies on immunological paralysis. VI. Thymic-independence of tolerance and immunity to type 3 pneumococcal polysaccharide. Cell Immunol. 1971 Dec;2(6):614–626. doi: 10.1016/0008-8749(71)90009-8. [DOI] [PubMed] [Google Scholar]
- Howard J. G., Christie G. H., Courtenay B. M. Studies on immunological paralysis. IV. The relative contributions of continuous antibody neutralization and central inhibition to paralysis with type 3 pneumococcal polysaccharide. Proc R Soc Lond B Biol Sci. 1971 Sep 28;178(1053):417–438. doi: 10.1098/rspb.1971.0073. [DOI] [PubMed] [Google Scholar]
- LANDY M., TRAPANI R. J., CLARK W. R. Studies on the O antigen of Salmonella typhosa. III. Activity of the isolated antigen in the hemagglutination procedure. Am J Hyg. 1955 Jul;62(1):54–65. doi: 10.1093/oxfordjournals.aje.a119766. [DOI] [PubMed] [Google Scholar]
- LYON M. F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature. 1961 Apr 22;190:372–373. doi: 10.1038/190372a0. [DOI] [PubMed] [Google Scholar]
- Marchalonis J. J., Cone R. E., Atwell J. L. Isolation and partial characterization of lymphocyte surface immunoglobulins. J Exp Med. 1972 Apr 1;135(4):956–971. doi: 10.1084/jem.135.4.956. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Okumura K., Tada T. Regulation of homocytotropic antibody formation in the rat. 3. Effect of thymectomy and splenectomy. J Immunol. 1971 Apr;106(4):1019–1025. [PubMed] [Google Scholar]
- Okumura K., Tada T. Regulation of homocytotropic antibody formation in the rat. VI. Inhibitory effect of thymocytes on the homocytotropic antibody response. J Immunol. 1971 Dec;107(6):1682–1689. [PubMed] [Google Scholar]
- 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]
- Seligmann M., Fudenberg H. H., Good R. A. A proposed classification of primary immunologic deficiencies. Am J Med. 1968 Dec;45(6):817–825. doi: 10.1016/0002-9343(68)90180-0. [DOI] [PubMed] [Google Scholar]
- Siskind G. W., Benacerraf B. Cell selection by antigen in the immune response. Adv Immunol. 1969;10:1–50. doi: 10.1016/s0065-2776(08)60414-9. [DOI] [PubMed] [Google Scholar]
- 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]
- Unanue E. R., Grey H. M., Rabellino E., Campbell P., Schmidtke J. Immunoglobulins on the surface of lymphocytes. II. The bone marrow as the main source of lymphocytes with detectable surface-bound immunoglobulin. J Exp Med. 1971 Jun 1;133(6):1188–1198. doi: 10.1084/jem.133.6.1188. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vitetta E. S., Baur S., Uhr J. W. Cell surface immunoglobulin. II. Isolation and characterization of immunoglobulin from mouse splenic lymphocytes. J Exp Med. 1971 Jul 1;134(1):242–264. doi: 10.1084/jem.134.1.242. [DOI] [PMC free article] [PubMed] [Google Scholar]