Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Binding of sheep erythrocytes in chronic lymphocytic leukemias of B-cell origin

  • 16 Accesses

  • 11 Citations


Two patients with B chronic lymphocytic leukemia having leukemic cells that bind sheep red blood cells by different mechanisms are described. In the first case, rosette formation was mediated by the anti-sheep erythrocyte activity of a monoclonal surface IgMk, related to Forssman antigen. In the second, E-rosette formation was found to be independent of both surface immunoglobulins and the classic E-rosette receptor since the leukemic cells were recognized neither by the OKT-11 monoclonal antibody nor by other markers specific for T-cell lineage. Evaluation of these rare cases emphasizes that detection of surface immunoglobulins and spontaneous rosetting are not sufficient for the characterization of leukemic clones and raises some doubts concerning the use of available surface markers in the characterization of lymphoproliferative disorders.

This is a preview of subscription content, log in to check access.


  1. 1.

    Aisenberg AC, Bloch KJ: Immunoglobulins on the surface of neoplastic lymphocytes. N Engl J Med 287:272–276, 1972

  2. 2.

    Preud'homme JL, Seligmann M: Surface bound immunoglobulins as a cell marker in human lymphoproliferative diseases. Blood 40:777–794, 1972

  3. 3.

    Shevach EM, Herberman RB, Frank MM, Green I: Receptors for complement and immunoglobulin on human leukaemic cells and human lymphoblastoid cell lines. J. Clin Invest 51:1933–1938, 1972

  4. 4.

    Catovsky D, Cherchi M, Okos A, Hegde U, Galton DAG: Mouse red cell rosettes in B-lymphoproliferative disorders. Br J Haematol 33:173–177, 1976

  5. 5.

    Hoffbrand A, Janossy G, Ganeshaguru K, Greaves MF: Multiparameter studies in lymphoid leukaemias. Am J Clin Pathol 72:736–745, 1979

  6. 6.

    Aisenberg AC: Current concepts: Cell-surface markers in lymphoproliferative disease. N Engl J Med 304:331–336, 1981

  7. 7.

    Brouet JC, Prieur AM: Membrane markers on chronic lymphocytic leukaemia cells: A B cell leukaemia with rosettes due to anti-sheep erythrocytes antibody activity of the membrane bound IgM and a T cell leukaemia with surface Ig. Clin Immunol Immunopathol 2:481–487, 1974

  8. 8.

    Hsu CCS, Marti GE, Schrek R, Williams RG Jr: Lymphocytes bearing B- and T-cell markers in patient with lymphosarcoma cell leukaemia. Clin Immunol Immunopathol 3:385–395, 1975

  9. 9.

    Singh AK, Vaughan-Smith S, Sawyer B, O'Connor TWE, Thomson AER, Wetherley-Mein G: Cell studies in prolymphocytic leukaemia. Br J Haematol. 40:587–596, 1978

  10. 10.

    Burns GF, Worman CP, Cawley JC: Fluctuations in the T and B characteristics of two cases of T-cell hairy-cell leukaemia. Clin Exp Immunol 39:76–82, 1980

  11. 11.

    Beck JD, Koziner B, Mertelsmann R, Platsoucas CD, Clarkson B, Good RA: B cells from a patient with chronic lymphocytic leukemia bind to sheep erythrocytes: An immunological analysis. Clin Immunol Immunopathol 16:233–237, 1980

  12. 12.

    Bergmann L, Mitrou PS, Rogge H: Surface IgMk of prolymphocytic leukaemia cells with antibody activity to surface antigens of sheep and guinea-pig red blood cells. Br J Haematol 48:103–110, 1981

  13. 13.

    Bertoglio J, Robert M, Noel B, Portoukalian J, Doré JF: Cells from a chronic lymphocytic leukaemia patient display surface immunoglobulins specific for Forssman antigen. Clin Immunol Immunopathol 19:325–329, 1981

  14. 14.

    Mitrou PS, Bergman L, Holloway K, Zerth G: E-rosette formation in B-cell lympathic leukaemias induced by binding activity of monoclonal surface immunoglobulins to sheep red blood cells. Clin Immunol Immunopathol 20:346–353, 1981

  15. 15.

    Bach JF: Evaluation of T-cells and thymic serum factors in man using the rosette technique. Transplant Rev 16:196–217, 1973

  16. 16.

    Pandolfi F, Strong DM, Slease RB, Smith ML, Ortaldo JR, Herberman RB: Characterization of a suppressor T-cell chronic lymphocytic leukemia with ADCC but not NK activity. Blood 56:653–660, 1980

  17. 17.

    Semenzato G, Milano A, Pezzutto A, Basso G, Cocito MG, Amadori G, Gasparotto G: D cells with cytotoxic activity in acute lymphoblastic leukaemia. Clin Immunol Immunopathol 16:238–244, 1980

  18. 18.

    Janossy G, Thomas JA, Pizzolo G, Granger SM, McLaughlin J, Habeshaw JA, Stansfeld AG, Sloane J: Immunohistological diagnosis of lymphoproliferative diseases by selected combinations of antisera and monoclonal antibodies. Br J Cancer 42:224–242, 1980

  19. 19.

    Pichler WJ, Broder S: Fc-IgM and Fc-IgG receptors on human circulating B lymphocytes. J Immunol 121:887–890, 1978

  20. 20.

    Foa R, Catovsky D: T-lymphocyte colonies in normal blood, bone marrow and lymphoproliferative disorders. Clin Exp Immunol 36:488–495, 1979

  21. 21.

    Pandolfi F, Paganelli R, Sirianni MC, D'Amelio R, Aiuti F: Rosette formation with mouse erythrocytes by lymphocytes from normal donors and patients with various diseases. Z Immunol Forsch 155:378–386, 1979

  22. 22.

    Fauci AS, Pratt KR: Polyclonal activation of bone marrowderived lymphocytes from human peripheral blood measured by a direct plaque-forming cell assay. Proc Natl Acad Sci USA 73:3676–3680, 1976

  23. 23.

    Heyman B, Andrighetto GC, Wigzell H: Antigen-dependent IgM-mediated enhancement of the sheep erythrocyte response in mice. Evidence for induction of B cells with specificities other than that of the injected antibodies. J Exp Med 155:994–1009, 1982

  24. 24.

    Reinherz EL, Schlossman SF: The differentiation and function of human T lymphocytes. Cell 19:821–827, 1980

  25. 25.

    Beverly PCL, Callard RE: Distinctive functional characteristics of human “T” lymphocytes defined by E rosetting or a monoclonal anti-T cell antibody. Eur J Immunol 11:329, 1981

  26. 26.

    Wang CY, Good RA, Ammirati P, Dymbort G, Evans RL: Identification of a p 69/71 complex expressed on human T cells sharing determinants with B-type chronic lymphatic leukemic cells. J Exp Med 151:1539–1544, 1980

  27. 27.

    Haynes BF, Mann DL, Hemler ME, Schroer JA, Shelhamer JH, Eisenbarth GS, Strominger JL, Thomas CA, Motowski H, Fauci AS: Characterization of a monoclonal antibody that defines an immunoregulatory T cell subset for immunoglobulin synthesis in humans. Proc Natl Acad Sci USA 77:2914–2918, 1980

  28. 28.

    Verbi W, Greaves MF, Kowbek K, Janossy G, Kung P, Goldstein G: OKT-11 and OKT-11A: Monoclonal antibodies with pan T reactivity which block sheep erythrocyte “receptors” on T cells. Eur J Immunol 12:81–86, 1982

  29. 29.

    Gelfand EW, Chechik BE: Unmasking the heterogeneity of acute lymphoblastic leukaemia. N Engl J Med 294:275–277, 1976

  30. 30.

    Dimitriou A, Haynes BF, Fauci AS: Activation of human B lymphocytes. XIV. Characterization of the precursor of the pokeweek mitogen-induced anti-sheep red blood cell plaqueforming cell. J Immunol 123:890–895, 1979

  31. 31.

    Aisenberg AC, Bloch KJ, Wilkes BM: Malignant lymphoma with dual B and T cell markers. Analysis of the neoplastic cells with monoclonal antibodies directed against T cell subsets. J Exp Med 154:1709–1714, 1981

  32. 32.

    Boumsell L, Bernard A, Lepage V, Degos L, Lemerle J, Dausset J: Some chronic lymphocytic leukemia cells bearing surface immunoglobulins share determinants with T cells. Eur J Immunol 8:900–904, 1978

  33. 33.

    Brochier J, Bouveret E, Vuvan H, Andary M, Clot J: Study of human B and T lymphocytes with heterologous antisera. V. Common antigens shared by T and B cells. Thymus 1:311–318, 1980

  34. 34.

    Boumsell L, Coppin H, Pham D, Raynal B, Lemerle J, Dausset J, Bernard A: An antigen shared by a human T cell subset and a B cell chronic lymphocytic leukemic cells. J Exp Med 152:229–234, 1980

  35. 35.

    Martin PJ, Hansen JA, Nowinski RC, Brown MA: A new human T-cell differentiation antigen: unexpected expression on chronic lymphocytic leukemia cells. Immunogenetics 11:429–439, 1980

  36. 36.

    Royston I, Majda JA, Baird SM, Meserve BL, Griffiths JC: Human T cell antigens defined by monoclonal antibodies: The 65,000-dalton antigen of T cells (T65) is also found on chronic lymphocytic leukaemia cells bearing surface immunoglobulins. J Immunol 125:725–731, 1980

  37. 37.

    Aisenberg AC: Cell-surface markers in lymphoproliferative disease. N Engl J Med 304:1302–1304, 1981

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Semenzato, G., Pizzolo, G., Gerosa, F. et al. Binding of sheep erythrocytes in chronic lymphocytic leukemias of B-cell origin. J Clin Immunol 2, 296–302 (1982).

Download citation

Key words

  • Chronic lymphocytic leukemia
  • E receptors
  • antisheep antibody activity
  • surface immunoglobulins