Transmembrane control of the receptors on normal and tumor cells: I. Cytoplasmic influence over cell surface components☆

The immunoglobulins which are present on the membrane of B lymphocytes of different species are mobile in the plane of the membrane itself.



This mobility results in the formation of spots of immunoglobulins when the cells are treated with divalent antibodies against immunoglobulins; the spots then combine into polar caps.



The process of spot formation is not inhibited by different substances that inhibit cell metabolism, but is markedly inhibited in the cold.



The formation of caps is followed by the disappearance of immunoglobulins from the cell membrane but, if the cells are not left in contact with the anti-immunoglobulin antiserum, there is a rapid resynthesis of new membrane immunoglobulins. It appears that the percentage of lymphocytes that resynthesize immunoglobulins is identical to that of cells originally carrying immunoglobulins, but the amount of surface immunoglobulins of each cell is increased after antiserum treatment. Many other membrane antigens behave in a similar way after treatment with the corresponding antisera; the possible role of the mobility of membrane proteins for the immunological functions of lymphocytes is discussed.

The dynamic state of the lymphocyte membrane. Factors affecting the distribution and turnover of surface immunoglobulins.

Publisher Summary This chapter describes membrane immunoglobulins and antigen receptors on B and T lymphocytes. There are several qualitative and quantitative distinctions between T-cell and B-cell M-Ig that may explain many of the apparent differences in reactivity of these cells without requiring the existence of a different set of V genes or non-Ig receptors in T cells. Both T and B cells derive from hematopoietic, precursor, stem cells by antigen-independent differentiation. This involves the activation of L-chain and p-type H-chain genes in both cell types. The T-cell and B-cell M-Ig differ primarily in density per cell and possibly in relative exposure on the cell surface with much of the H-chain Fc region inaccessible on T cells. Moreover, the antigen-recognition receptor of both T and B cells involves their M-Ig. On B cells, the receptor is solely the M-Ig, whereas on T cells it is suggested that the specificity of recognition controlled primarily by the M-Ig and binding of antigen to the cell can solely be by the M-Ig receptor. Finally, the activation of the T cell requires an additional interaction of the antigen with another ceIl surface structure that is coded for by a polymorphic H-2 linked gene.

Membrane immunoglobulins and antigen receptors on B and T lymphocytes.

The ultrastructural distribution of membrane-bound immunoglobulin (Ig) on mouse spleen lymphocytes has been studied by labeling the surface Ig with anti-mouse Ig antibody conjugated to ferritin (FT). The distribution is temperature-dependent. At 0 °C – 4 °C FT appears distributed in small clusters over the entire surface, whereas at 20 °C – 22 °C, in the great majority of the labeled cells, it is concentrated over one pole. This pole corresponds to that part of the cell which contains the Golgi complex and most of the cellular organelles, and which forms the uropod in moving lymphocytes. This polar redistribution is accompanied by endocytosis of part of the labeled membrane.



The redistribution of label occurring at room temperature indicates that labeled and unlabeled components of the plasma membrane can segregate from each other and suggests that plasma membrane is fluid at room temperature. The diffuse distribution found at 0 °C – 4 °C is probably close (although not identical) to the distribution in vivo before labeling, while the polar distribution at higher temperature is probably induced by the cross-linking of the surface Ig molecules by the antibody-FT conjugate and by a metabolically-dependent flow of the aggregates towards the “tail” of the lymphocyte. The mechanism involved is considered to be the same mechanism responsible for membrane flow during cell movement. A detailed model of the structure and rheological properties of the lymphocyte membrane is proposed, which can explain the present results and those of others concerning the behavior of surface components of lymphocytes and other cells.

Distribution of immunoglobulin on the surface of mouse lymphoid cells as determined by immunoferritin electron microscopy. Antibody-induced, temperature-dependent redistribution and its implications for membrane structure.

By means of immunofluorescence technique, lymphocytes with surface-bound immunoglobulin were detected in the blood of normal humans F(ab')2, IgM, IgG, IgA, the four IgG subclasses, and the Gm markers Gm(f) and Gm(Z) were demonstrated on cells. IgM was the dominating class, and IgG2 the dominating IgG subclass. The data suggest that the Ig on any one cell belongs to a single class and IgG subclass. Very few lymphocytes stained for antigens on the C-terminal half of ihe IgG molecule. Ig-positive lymphocytes were also demonstrated in cord blood and in spleen cell suspensions. An almost total lack of Ig-positive lymphocytes was demonstrated in the blood of 8 patients with severe hypogammaglobulinemia. The Ig-positive lymphocytes are thought to be analogous to B-lymphocytes in other species.

Surface-bound immunoglobulin on lymphocytes from normal and immunodeficient humans.

THE initiation of the immune response is believed to involve the recognition of antigen by specific receptors on the surface of lymphocytes. The transformation of rabbit and human lymphocytes by antisera to immunoglobulins1–3, the blocking of antigen binding by lymphocytes using anti-immunoglobulins4 and the inhibition of antigen induced lymphocyte transformation by anti-light chain serum5 suggest that such receptors are immunoglobulin in nature or at least possess immunoglobulin determinants. We have now obtained direct evidence for the presence of immunoglobulin determinants on the surface of rabbit lymphocytes by autoradiography using radio-labelled anti-allotype sera.

Immunoglobulin allotypic determinants on rabbit lymphocytes.

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Immunoglobulin allotypic determinants on rabbit lymphocytes.