Skip to main content
British Journal of Cancer logoLink to British Journal of Cancer
. 1979 Jul;40(1):11–34. doi: 10.1038/bjc.1979.137

Surface phenotyping, histology and the nature of non-Hodgkin lymphoma in 157 patients.

J A Habeshaw, P F Catley, A G Stansfeld, R L Brearley
PMCID: PMC2009956  PMID: 314300

Abstract

In a study of 157 patients with lymphoid malignancy, the phenotype of the tumour cells was correlated with the histological classification of the tumour using the Rappaport and the Kiel classifications. The markers used included E, Fc gamma, Fc micron (IgM) and C3d rosetting, estimation of SIg and CyIg, and tests for the expression of HTLA, Ia and ALL. Repeat biopsy specimens were studied in 23 of these patients. The phenotypic features of lymphoblastic malignancy indicated B-cell, T-cell and ALL-positive null-cell tumours in this group. Immunoblastic lymphomas were predominantly of non-capping B-cell type, but T-cell immunoblastic lymphoma occurred in 2 patients. Immunoblastic lymphomas of receptor-silent cells occur, and are ALL- and HTLA-negative. In the category of diffuse, poorly differentiated lymphocytic lymphomas, most cases are of centroblastic and centrocytic tumour of diffuse type, but pure centrocytic tumours and centroblastic tumours occur. The dominant phenotype in this group is of B cells expressing C3d receptors. Nodular poorly differentiated lymphocytic lymphomas (Rappaport) are classified as centroblastic and centrocytic follicular (Kiel) and most express SIg+ C3d+ phenotype. The frequency of this phenotype appeared the same in both diffuse and nodular poorly differentiated lymphocytic neoplasms. The Rappaport group of diffuse well-differentiated lymphocytic lymphoma includes 2 Kiel categories, malignant lymphoma lymphocytic, and malignant lymphoma lymphoplasmacytoid. Cells of the former tumour were considered to be immature B cells resembling those seen in CLL, and characteristically expressing SIg weakly, with a high frequency of single kappa light chain. Cells of the latter tumour are by contrast mature, and are related to the centroblastic and centrocytic follicular tumour by their histogenesis and phenotypic features. Repeat biopsy examinations indicate that T-cell predominance occurs in the prodromal phase of B-cell-predominant tumours of SIg+ C3d+ phenotype. It is concluded that non-Hodgkin lymphoma can be divided into 2 categories: (1) tumours of immature immunologically incompetent cells of lymphoblastic histology and with phenotypic features akin to T, B and Null-cell ALL, and (2) tumours of differentiated lymphocytes expressing the phenotypic features of B lymphocytes, with maturation arrested at one of several stages of an antigen-dependent immune response.

Full text

PDF
11

Selected References

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

  1. Baltimore D. Is terminal deoxynucleotidyl transferase a somatic mutagen in lymphocytes? Nature. 1974 Mar 29;248(447):409–411. doi: 10.1038/248409a0. [DOI] [PubMed] [Google Scholar]
  2. Barrett S. G., Schwade J. G., Ranken R., Kadin M. E. Lymphoblasts with both T and B markers in childhood leukemia and lymphoma. Blood. 1977 Jul;50(1):71–79. [PubMed] [Google Scholar]
  3. Bolhuis R. L., Nooyen A. J. Receptors for IgM and IgM-antigen complexes on human T-lymphocytes reacting with specific anti-human-T-cell antiserum. Immunology. 1977 Nov;33(5):679–687. [PMC free article] [PubMed] [Google Scholar]
  4. Braylan R. C., Jaffe E. S., Mann R. B., Frank M. M., Berard C. W. Surface receptors of human neoplastic lymphoreticular cells. Haematol Blood Transfus. 1977;20:47–53. doi: 10.1007/978-3-642-66639-1_5. [DOI] [PubMed] [Google Scholar]
  5. Brunning R. D., McKenna R. W., Bloomfield C. D., Coccia P., Gajl-Peczalska K. J. Bone marrow involvement in Burkitt's lymphoma. Cancer. 1977 Oct;40(4):1771–1779. doi: 10.1002/1097-0142(197710)40:4<1771::aid-cncr2820400456>3.0.co;2-5. [DOI] [PubMed] [Google Scholar]
  6. Chapel H. M., Ling N. R. Combined T and B lymphocyte marker test in lymphoproliferative disorders. Br J Haematol. 1977 Mar;35(3):367–371. doi: 10.1111/j.1365-2141.1977.tb00596.x. [DOI] [PubMed] [Google Scholar]
  7. Chiao J. W., Pantic V. S., Good R. A. Human peripheral lymphocytes bearing both B-cell complement receptors and T-cell characteristics for sheep erythrocytes detected by a mixed rosette method. Clin Exp Immunol. 1974 Dec;18(4):483–490. [PMC free article] [PubMed] [Google Scholar]
  8. Coffman R. L., Cohn M. The class of surface immunoglobulin on virgin and memory B lymphocytes. J Immunol. 1977 May;118(5):1806–1815. [PubMed] [Google Scholar]
  9. Davies A. J., Carter R. L., Leuchars E., Wallis V., Koller P. C. The morphology of immune reactions in normal, thymectomized and reconstituted mice. I. The response to sheep erythrocytes. Immunology. 1969 Jan;16(1):57–69. [PMC free article] [PubMed] [Google Scholar]
  10. Dickler H. B., Adkinson N. F., Jr, Terry W. D. Evidence for individual human peripheral blood lymphocytes bearing both B and T cell markers. Nature. 1974 Jan 25;247(5438):213–215. doi: 10.1038/247213a0. [DOI] [PubMed] [Google Scholar]
  11. Donlon J. A., Jaffe E. S., Braylan R. C. Terminal deoxynucleotidyl transferase activity in malignant lymphomas. N Engl J Med. 1977 Sep 1;297(9):461–464. doi: 10.1056/NEJM197709012970901. [DOI] [PubMed] [Google Scholar]
  12. Ferrarini M., Moretta L., Abrile R., Durante M. L. Receptors for IgG molecules on human lymphocytes forming spontaneous rosettes with sheep red cells. Eur J Immunol. 1975 Jan;5(1):70–72. doi: 10.1002/eji.1830050115. [DOI] [PubMed] [Google Scholar]
  13. Fukuhara S., Shirakawa S., Uchino H. Specific marker chromosome 14 in malignant lymphomas. Nature. 1976 Jan 22;259(5540):210–211. doi: 10.1038/259210a0. [DOI] [PubMed] [Google Scholar]
  14. Habeshaw J. A., Macaulay R. A., Stuart A. E. Correlation of surface receptors with histological appearance in 29 cases of non-Hodgkin lymphoma. Br J Cancer. 1977 Jun;35(6):858–867. doi: 10.1038/bjc.1977.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Habeshaw J. A., Stuart A. E. Cell receptor studies on seven cases of diffuse histiocytic malignant lymphoma (reticulum cell sarcoma). J Clin Pathol. 1975 Apr;28(4):289–297. doi: 10.1136/jcp.28.4.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Habeshaw J. A., Stuart A. E., Dewar A. E., Young G. Letter: IgM receptors on cells in Hodgkin's disease. Lancet. 1976 Apr 24;1(7965):916–916. doi: 10.1016/s0140-6736(76)92144-9. [DOI] [PubMed] [Google Scholar]
  17. Hann H. W., London W. T., Evans A. E. Lymphoblasts with T-cell markers in five girls with acute lymphocytic leukemia. Cancer. 1977 May;39(5):2001–2003. doi: 10.1002/1097-0142(197705)39:5<2001::aid-cncr2820390516>3.0.co;2-n. [DOI] [PubMed] [Google Scholar]
  18. Harris N. S. Plasma cell surface antigen on human blood lymphocytes. Nature. 1974 Aug 9;250(5466):507–509. doi: 10.1038/250507a0. [DOI] [PubMed] [Google Scholar]
  19. Hoffbrand A. V., Ganeshaguru K., Janossy G., Greaves M. F., Catovsky D., Woodruff R. K. Terminal deoxynucleotidyl-transferase levels and membrane phenotypes in diagnosis of acute leukaemia. Lancet. 1977 Sep 10;2(8037):520–523. doi: 10.1016/s0140-6736(77)90662-6. [DOI] [PubMed] [Google Scholar]
  20. Hoffmann M. K., Hämmerling U., Simon M., Oettgen H. F. Macrophage requirements of CR- and CR+ B lymphocytes for antibody production in vitro. J Immunol. 1976 May;116(5):1447–1451. [PubMed] [Google Scholar]
  21. Hämmerling U., Chin A. F., Abbott J. Ontogeny of murine B lymphocytes: sequence of B-cell differentiation from surface-immunoglobulin-negative precursors to plasma cells. Proc Natl Acad Sci U S A. 1976 Jun;73(6):2008–2012. doi: 10.1073/pnas.73.6.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hütteroth T. H., Litwin S. D., Cleve H. Cultured lymphoid cell lines from normal subjects: membrane associated immunoglobulins studied by the mixed antiglobulin reaction. Cell Immunol. 1972 Nov;5(3):446–458. doi: 10.1016/0008-8749(72)90071-8. [DOI] [PubMed] [Google Scholar]
  23. Jaffe E. S., Braylan R. C., Nanba K., Frank M. M., Berard C. W. Functional markers: a new perspective on malignant lymphomas. Cancer Treat Rep. 1977 Sep;61(6):953–962. [PubMed] [Google Scholar]
  24. Jaffe E. S., Shevach E. M., Frank M. M., Berard C. W., Green I. Nodular lymphoma--evidence for origin from follicular B lymphocytes. N Engl J Med. 1974 Apr 11;290(15):813–819. doi: 10.1056/NEJM197404112901501. [DOI] [PubMed] [Google Scholar]
  25. Janossy G., Goldstone A. H., Capellaro D., Greaves M. F., Kulenkampff J., Pippard M., Welsh K. Differentiation linked expression of p28,33 (Ia-like) structures on human leukaemic cells. Br J Haematol. 1977 Nov;37(3):391–402. doi: 10.1111/j.1365-2141.1977.tb01010.x. [DOI] [PubMed] [Google Scholar]
  26. Jerne N. K. The somatic generation of immune recognition. Eur J Immunol. 1971 Jan;1(1):1–9. doi: 10.1002/eji.1830010102. [DOI] [PubMed] [Google Scholar]
  27. Kearney J. F., Cooper M. D., Lawton A. R. B lymphocyte differentiation induced by lipopolysaccharide. III. Suppression of B cell maturation by anti-mouse immunoglobulin antibodies. J Immunol. 1976 Jun;116(6):1664–1668. [PubMed] [Google Scholar]
  28. Kearney J. F., Klein J., Bockman D. E., Cooper M. D., Lawton A. R. B cell differentiation induced by lipopolysaccharide. V. Suppression of plasma cell maturation by anti-mu: mode of action and characteristics of suppressed cells. J Immunol. 1978 Jan;120(1):158–166. [PubMed] [Google Scholar]
  29. Kersey J. H., Nesbit M. E., Luckasen J. R., Hallgren H. M., Sabad A., Yunis E. J., Gajl-Peczalska K. J. Acute lymphoblastic leukemic and lymphoma cells with thymus-derived (T) markers. Mayo Clin Proc. 1974 Aug;49(8):584–587. [PubMed] [Google Scholar]
  30. Kung P. C., Long J. C., McCaffrey R. P., Ratliff R. L., Harrison T. A., Baltimore D. Terminal deoxynucleotidyl transferase in the diagnosis of leukemia and malignant lymphoma. Am J Med. 1978 May;64(5):788–794. doi: 10.1016/0002-9343(78)90518-1. [DOI] [PubMed] [Google Scholar]
  31. Lewis G. K., Ranken R., Nitecki D. E., Goodman J. W. Murine B-cell subpopulations responsive to T-dependent and T-independent antigens. J Exp Med. 1976 Aug 1;144(2):382–397. doi: 10.1084/jem.144.2.382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Louie S., Schwartz R. S. Immunodeficiency and the pathogenesis of lymphoma and leukemia. Semin Hematol. 1978 Apr;15(2):117–138. [PubMed] [Google Scholar]
  33. Lukes R. J., Collins R. D. Immunologic characterization of human malignant lymphomas. Cancer. 1974 Oct;34(4 Suppl):suppl–suppl:1503. doi: 10.1002/1097-0142(197410)34:8+<1488::aid-cncr2820340822>3.0.co;2-c. [DOI] [PubMed] [Google Scholar]
  34. Manolov G., Manolova Y. Marker band in one chromosome 14 from Burkitt lymphomas. Nature. 1972 May 5;237(5349):33–34. doi: 10.1038/237033a0. [DOI] [PubMed] [Google Scholar]
  35. McCaffrey R., Harrison T. A., Parkman R., Baltimore D. Terminal deoxynucleotidyl transferase activity in human leukemic cells and in normal human thymocytes. N Engl J Med. 1975 Apr 10;292(15):775–780. doi: 10.1056/NEJM197504102921504. [DOI] [PubMed] [Google Scholar]
  36. McCaw B. K., Hecht F., Harnden D. G., Teplitz R. L. Somatic rearrangement of chromosome 14 in human lymphocytes. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2071–2075. doi: 10.1073/pnas.72.6.2071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. McConnell I., Hurd C. M. Lymphocyte receptors. II. Receptors for rabbit IgM on human T lymphocytes. Immunology. 1976 Jun;30(6):835–839. [PMC free article] [PubMed] [Google Scholar]
  38. Moretta L., Mingari M. C., Moretta A., Lydyard P. M. Receptors for IgM are expressed on acute lymphoblastic leukemic cells having T-cell characteristics. Clin Immunol Immunopathol. 1977 May;7(3):405–409. doi: 10.1016/0090-1229(77)90075-7. [DOI] [PubMed] [Google Scholar]
  39. Nieuwenhuis P., Keuning F. J. Germinal centres and the origin of the B-cell system. II. Germinal centres in the rabbit spleen and popliteal lymph nodes. Immunology. 1974 Mar;26(3):509–519. [PMC free article] [PubMed] [Google Scholar]
  40. Nieuwenhuis P., van Nouhuijs C. E., Eggens J. H., Keuning F. J. Germinal centres and the origin of the B-cell system. I. Germinal centres in the rabbit appendix. Immunology. 1974 Mar;26(3):497–507. [PMC free article] [PubMed] [Google Scholar]
  41. Pearl E. R., Vogler L. B., Okos A. J., Crist W. M., Lawton A. R., 3rd, Cooper M. D. B lymphocyte precursors in human bone marrow: an analysis of normal individuals and patients with antibody-deficiency states. J Immunol. 1978 Apr;120(4):1169–1175. [PubMed] [Google Scholar]
  42. Salmon S. E., Seligmann M. B-cell neoplasia in man. Lancet. 1974 Nov 23;2(7891):1230–1233. doi: 10.1016/s0140-6736(74)90748-x. [DOI] [PubMed] [Google Scholar]
  43. Sidman C. L., Unanue E. R. Receptor-mediated inactivation of early B lymphocytes. Nature. 1975 Sep 11;257(5522):149–151. doi: 10.1038/257149a0. [DOI] [PubMed] [Google Scholar]
  44. Stein H. Immunchemische und immunzytologische Befunde bei Non-HODGKIN-Lymphomen. Hamatol Bluttransfus. 1976;18:167–183. [PubMed] [Google Scholar]
  45. Stein H., Petersen N., Gaedicke G., Lennert K., Landbeck G. Lymphoblastic lymphoma of convoluted or acid phosphatase type-a tumor of T precursor cells. Int J Cancer. 1976 Mar 15;17(3):292–295. doi: 10.1002/ijc.2910170303. [DOI] [PubMed] [Google Scholar]
  46. Stein H., Siemssen U., Lennert K. Complement receptor subtypes C3b and C3d in lymphatic tissue and follicular lymphoma. Br J Cancer. 1978 Apr;37(4):520–529. doi: 10.1038/bjc.1978.80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Stocker J. W. Tolerance induction in maturing B cells. Immunology. 1977 Mar;32(3):283–290. [PMC free article] [PubMed] [Google Scholar]
  48. Stuart A. E., Habeshaw J. A. Receptor studies on 19 cases of non-Hodgkin malignant lymphocytic lymphoma. Acta Haematol. 1976;55(3):160–168. doi: 10.1159/000208009. [DOI] [PubMed] [Google Scholar]
  49. Toben H. R., Smith R. G. T lymphocytes bearing complement receptors in a patient with chronic lymphocytic leukaemia. Clin Exp Immunol. 1977 Feb;27(2):292–302. [PMC free article] [PubMed] [Google Scholar]
  50. Vogler L. B., Crist W. M., Bockman D. E., Pearl E. R., Lawton A. R., Cooper M. D. Pre-B-cell leukemia. A new phenotype of childhood lymphoblastic leukemia. N Engl J Med. 1978 Apr 20;298(16):872–878. doi: 10.1056/NEJM197804202981603. [DOI] [PubMed] [Google Scholar]
  51. Wernet P., Betsch C., Barth P., Jaramillo S., Schunter F., Waller H. D., Wilms K. Human Ia alloantigens as cell-differentiation markers of normal and pathologic leukocyte surfaces. Scand J Immunol. 1977;6(5):563–574. doi: 10.1111/j.1365-3083.1977.tb02121.x. [DOI] [PubMed] [Google Scholar]

Articles from British Journal of Cancer are provided here courtesy of Cancer Research UK

RESOURCES