Abstract
Evidence is presented for the existence on all B lymphocytes, but not on T lymphocytes, of a membrane-associated receptor for antibody. The receptor was detected by a radioautographic technique in which lymphoid cells were incubated with antibody followed by the corresponding radioiodinated antigen. The ease with which antibody eluted during washing indicated that the bond between antibody and cell was weak. The formation of an antibody-antigen complex on the cell surface, however, stabilized the bond and permitted accurate quantitation of cells with adherent antibody. The ability of several combinations of antibody and antigen to adhere to the cells demonstrated the nonspecificity of the phenomenon and emphasized the need for care in interpretation of antigen-binding studies particularly when immune cells are being used. The identity of antibody-binding lymphocytes was established by two different approaches. In the first, mouse lymphocyte populations greatly enriched for either T cells or B cells were examined. Their T cell content was assessed by means of well-established markers such as the θ C3H isoantigen. When this was compared with the number of antibody-binding cells, an inverse relationship was obtained in each instance; thus almost all thoracic duct cells from athymic mice labeled with an immune complex although none were θ positive. The striking reduction in antibody-binding cells observed in bursectomized chickens provided a second and independent line of evidence suggesting that B cells, not T cells, bind antibody. The ability of B cells from primed animals to bind antibody in vivo made it important to test whether this phenomenon was related to the carriage of immunological memory. No correlation was, however, found between membrane-bound antibody and memory. It was proposed that the existence of a receptor of this kind may provide a rational explanation for antibody-dependent killing of target cells and may prove of importance in antigen concentration particularly during the secondary response.
Full Text
The Full Text of this article is available as a PDF (998.3 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- ADA G. L., NOSSAL G. J., PYE J., ABBOT A. ANTIGENS IN IMMUNITY. I. PREPARATION AND PROPERTIES OF FLAGELLAR ANTIGENS FROM SALMONELLA ADELAIDE. Aust J Exp Biol Med Sci. 1964 Jun;42:267–282. [PubMed] [Google Scholar]
- Basten A., Miller J. F., Warner N. L., Pye J. Specific inactivation of thymus-derived (T) and non-thymus-derived (B) lymphocytes by 125I-labelled antigen. Nat New Biol. 1971 May 26;231(21):104–106. doi: 10.1038/newbio231104a0. [DOI] [PubMed] [Google Scholar]
- Basten A., Warner N. L., Mandel T. A receptor for antibody on B lymphocytes. II. Immunochemical and electron microscopy characteristics. J Exp Med. 1972 Mar 1;135(3):627–642. doi: 10.1084/jem.135.3.627. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bianco C., Nussenzweig V. Theta-bearing and complement-receptor lymphocytes are distinct populations of cells. Science. 1971 Jul 9;173(3992):154–156. doi: 10.1126/science.173.3992.154. [DOI] [PubMed] [Google Scholar]
- Bianco C., Patrick R., Nussenzweig V. A population of lymphocytes bearing a membrane receptor for antigen-antibody-complement complexes. I. Separation and characterization. J Exp Med. 1970 Oct 1;132(4):702–720. doi: 10.1084/jem.132.4.702. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Byrt P., Ada G. L. An in vitro reaction between labelled flagellin or haemocyanin and lymphocyte-like cells from normal animals. Immunology. 1969 Oct;17(4):503–516. [PMC free article] [PubMed] [Google Scholar]
- Cunningham A. J., Szenberg A. Further improvements in the plaque technique for detecting single antibody-forming cells. Immunology. 1968 Apr;14(4):599–600. [PMC free article] [PubMed] [Google Scholar]
- DULBECCO R., VOGT M. Plaque formation and isolation of pure lines with poliomyelitis viruses. J Exp Med. 1954 Feb;99(2):167–182. doi: 10.1084/jem.99.2.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hulliger L., Blazkovec A. A. A simple and efficient method of separating peripheral-blood leucocytes for in-vitro studies. Lancet. 1967 Jun 17;1(7503):1304–1305. doi: 10.1016/s0140-6736(67)91596-6. [DOI] [PubMed] [Google Scholar]
- Iványi J. Early 7S antibody--antigen complexes with affinity to spleen cells in chickens immunized with a low dose of human serum albumin. Immunology. 1970 Oct;19(4):629–635. [PMC free article] [PubMed] [Google Scholar]
- KERN M., EISEN H. N. The effect of antigenic stimulation on incorporation of phosphate and methionine into proteins of isolated lymph node cells. J Exp Med. 1959 Aug 1;110(2):207–219. doi: 10.1084/jem.110.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MacLennan I. C., Harding B. Failure of certain cytotoxic lymphocytes to respond mitotically to phytohaemagglutinin. Nature. 1970 Sep 19;227(5264):1246–1248. doi: 10.1038/2271246a0. [DOI] [PubMed] [Google Scholar]
- MacLennan I. C., Loewi G., Harding B. The role of immunoglobulins in lymphocyte-mediated cell damage, in vitro. I. Comparison of the effects of target cell specific antibody and normal serum factors on cellular damage by immune and non-immune lymphocytes. Immunology. 1970 Mar;18(3):397–404. [PMC free article] [PubMed] [Google Scholar]
- Miller J. F., Mitchell G. F. Cell to cell interaction in the immune response. I. Hemolysin-forming cells in neonatally thymectomized mice reconstituted with thymus or thoracic duct lymphocytes. J Exp Med. 1968 Oct 1;128(4):801–820. doi: 10.1084/jem.128.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller J. F., Sprent J., Basten A., Warner N. L., Breitner J. C., Rowland G., Hamilton J., Silver H., Martin W. J. Cell-to-cell interaction in the immune response. VII. Requirement for differentiation of thymus-derived cells. J Exp Med. 1971 Nov 1;134(5):1266–1284. doi: 10.1084/jem.134.5.1266. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller J. F., Sprent J. Thymus-derived cells in mouse thoracic duct lymph. Nat New Biol. 1971 Apr 28;230(17):267–270. doi: 10.1038/newbio230267a0. [DOI] [PubMed] [Google Scholar]
- Miller J. F., Warner N. L. The immune response of normal, irradiated and thymectomized mice to fowl immunoglobulin G as detected by a hemolytic plaque technique. Int Arch Allergy Appl Immunol. 1971;40(1):59–71. doi: 10.1159/000230395. [DOI] [PubMed] [Google Scholar]
- Modabber F., Sercarz E. E. Antigen binding and the immune response. II. The large number of antigen-binding cells in primed animals. Proc Soc Exp Biol Med. 1970 Nov;135(2):400–405. doi: 10.3181/00379727-135-35061. [DOI] [PubMed] [Google Scholar]
- Nossal G. J., Ada G. L., Austin C. M., Pye J. Antigens in immunity. 8. Localization of 125-I-labelled antigens in the secondary response. Immunology. 1965 Oct;9(4):349–357. [PMC free article] [PubMed] [Google Scholar]
- Nossal G. J., Austin C. M., Pye J., Mitchell J. Antigens in immunity. XII. Antigen trapping in the spleen. Int Arch Allergy Appl Immunol. 1966;29(4):368–383. [PubMed] [Google Scholar]
- Perlmann P., Perlmann H. Contactual lysis of antibody-coated chicken erythrocytes by purified lymphocytes. Cell Immunol. 1970 Sep;1(3):300–315. doi: 10.1016/0008-8749(70)90051-1. [DOI] [PubMed] [Google Scholar]
- 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]
- Rabellino E., Colon S., Grey H. M., Unanue E. R. Immunoglobulins on the surface of lymphocytes. I. Distribution and quantitation. J Exp Med. 1971 Jan 1;133(1):156–167. doi: 10.1084/jem.133.1.156. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raff M. C., Owen J. J. Thymus-derived lymphocytes: their distribution and role in the development of peripheral lymphoid tissues of the mouse. Eur J Immunol. 1971 Jan;1(1):27–30. doi: 10.1002/eji.1830010105. [DOI] [PubMed] [Google Scholar]
- Sinclair N. R., Lees R. K., Chan P. L., Khan R. H. Regulation of the immune response. II. Further studies on differences in ability of F(ab')2 and 7S antibodies to inhibit an antibody response. Immunology. 1970 Jul;19(1):105–116. [PMC free article] [PubMed] [Google Scholar]
- Sprent J., Miller J. F. Activation of thymus cells by histocompatibility antigens. Nat New Biol. 1971 Sep 15;234(50):195–198. doi: 10.1038/newbio234195a0. [DOI] [PubMed] [Google Scholar]
- Warner N. L., Ovary Z., Kantor F. S. Delayed hypersensitivity reactions in normal and bursectomized chickens. Int Arch Allergy Appl Immunol. 1971;40(4-5):719–728. doi: 10.1159/000230454. [DOI] [PubMed] [Google Scholar]