Abstract
This study relateds the cytologic types of the classification of malignant lymphoma of Lukes and Collins to the results of immunologic surface marker studies as part of a systematic multiparameter study of 299 cases of non-Hodgkin lymphomas. The results support the hypothesis that malignant lymphomas are neoplasms of the immune system and involve the B- and T-cell systems and, rarely, histiocytes. The morphologic features of the cytologic types of Lukes and Collins are predictive of the subtypes of lymphoma and considerably more effective than the immunologic surface marker techniques in identifying homogeneous groups. There are considerable methodologic and interpretive problems that are evaluated in detail. The verification of the B- and T-cell subtypes of the Lukes and Collins classification indicates that the time has come to change from the terminology and classification of lymphomas of the past to a modern immunologic approach.
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- Abdou N. L., Alavi J. B., Abdou N. I. Human bone marrow lymphocytes: B and T cell precursors and subpopulations. Blood. 1976 Mar;47(3):423–430. [PubMed] [Google Scholar]
- Aisenberg A. C., Long J. C. Lymphocyte surface characteristics in malignant lymphoma. Am J Med. 1975 Mar;58(3):300–306. doi: 10.1016/0002-9343(75)90595-1. [DOI] [PubMed] [Google Scholar]
- Alexander M., Glatstein E. J., Gordon D. S., Daniels J. R. Combined modality treatment for oat cell carcinoma of the lung: a randomized trial 1,2,3. Cancer Treat Rep. 1977 Jan-Feb;61(1):1–6. [PubMed] [Google Scholar]
- Atsaldi G., Astaldi G. C., Topuz U., Guarina L. Lymphocyte immunological patterns in leukaemia: a review. Haematologia (Budap) 1975;9(1-2):21–33. [PubMed] [Google Scholar]
- Bach J. F., Judet C., Arce S., Dormont J. Exploration de la fonction thymique chez l'homme. II. Le phénomène des "rosettes-mouton", marqueur des lymphocytes T chez l'homme. Nouv Presse Med. 1974 Mar 16;3(11):655–660. [PubMed] [Google Scholar]
- Billing R., Ting A., Terasaki P. I. Human B-lymphocyte antigens expressed by lymphocytic and myelocytic leukemia cells. II. Detection by human anti-B-cell alloantisera. J Natl Cancer Inst. 1977 Feb;58(2):199–203. doi: 10.1093/jnci/58.2.199. [DOI] [PubMed] [Google Scholar]
- Birnbaum G. Numbers of rosette formine cells in human peripheral blood. Cell Immunol. 1976 Feb;21(2):371–378. doi: 10.1016/0008-8749(76)90066-6. [DOI] [PubMed] [Google Scholar]
- Bobrove A. M., Fuks Z., Strober S., Kaplan H. S. Quantitation of T and B lymphocytes and cellular immune function in Hodgkin's disease. Cancer. 1975 Jul;36(1):169–179. doi: 10.1002/1097-0142(197507)36:1<169::aid-cncr2820360115>3.0.co;2-z. [DOI] [PubMed] [Google Scholar]
- Bouvet J. P., Buffe D., Oriol R., Liacopoulos P. Two myeloma globulins IgG1-kappa and IgG1-lambda, from a single patient (Im). II. Their common cellular origin as revealed by immunofluorescence studies. Immunology. 1974 Dec;27(6):1095–1101. [PMC free article] [PubMed] [Google Scholar]
- Braylan R. C., Jaffe E. S., Berard C. W. Malignant lymphomas: current classification and new observations. Pathol Annu. 1975;10:213–270. [PubMed] [Google Scholar]
- Browne O., Bell J., Holland P. D., Thornes R. D. Letter: Plasmapheresis and immunostimulation. Lancet. 1976 Jul 10;2(7976):96–96. doi: 10.1016/s0140-6736(76)92311-4. [DOI] [PubMed] [Google Scholar]
- Case records of the Masschusetts General Hospital. Weekly clinicopathological exercises. Case 30-1977. N Engl J Med. 1977 Jul 28;297(4):206–211. doi: 10.1056/NEJM197707282970409. [DOI] [PubMed] [Google Scholar]
- Catovsky D., Cherchi M., Okos A., Hegde U., Galton D. A. Mouse red-cell rosettes in B-lymphoproliferative disorders. Br J Haematol. 1976 Jun;33(2):173–177. doi: 10.1111/j.1365-2141.1976.tb03528.x. [DOI] [PubMed] [Google Scholar]
- Catovsky D., Miliani E., Okos A., Galton D. A. Clinical significance of T-cells in chronic lymphocytic leukaemia. Lancet. 1974 Sep 28;2(7883):751–752. doi: 10.1016/s0140-6736(74)90944-1. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Cohnen G., Brittinger G. Studies on human T lymphocyte rosette formation with human and sheep erythrocytes. Res Exp Med (Berl) 1975 Nov 26;166(1):1–13. doi: 10.1007/BF01851341. [DOI] [PubMed] [Google Scholar]
- Cordier G., Samarut C., Brochier J., Revillard J. P. Antibody-dependent cell cytoxicity (ADCC). Characterization of 'killer' cells in human lymphoid organs. Scand J Immunol. 1976;5(3):233–242. doi: 10.1111/j.1365-3083.1976.tb00274.x. [DOI] [PubMed] [Google Scholar]
- Cushman P., Khurana R. Marijuana and T lymphocyte rosettes. Clin Pharmacol Ther. 1976 Mar;19(3):310–317. doi: 10.1002/cpt1976193310. [DOI] [PubMed] [Google Scholar]
- Davey F. R., Goldberg J., Stockman J., Gottlieb A. J. Immunologic and cytochemical cell markers in non-Hodgkin's lymphomas. Lab Invest. 1976 Nov;35(5):430–438. [PubMed] [Google Scholar]
- De Préval C., Fougereau M. Specific interaction between VH and VL regions of human monoclonal immunoglobulins. J Mol Biol. 1976 Apr 15;102(3):657–678. doi: 10.1016/0022-2836(76)90340-5. [DOI] [PubMed] [Google Scholar]
- Eastham R. J., Mason J. M., Jennings B. R., Belew P. W., Maguda T. A. T-cell rosette test in squamous cell carcinoma of the head and neck. Arch Otolaryngol. 1976 Mar;102(3):171–175. doi: 10.1001/archotol.1976.00780080093013. [DOI] [PubMed] [Google Scholar]
- Fu S. M., Winchester R. J., Kunkel H. G. The occurrence of the HL-B alloantigens on the cells of unclassified acute lymphoblastic leukemias. J Exp Med. 1975 Nov 1;142(5):1334–1338. doi: 10.1084/jem.142.5.1334. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fuks Z., Glatstein E., Kaplan H. S. Patterns of presentation and relapse in the non-Hodgkin's lymphomata. Br J Cancer Suppl. 1975 Mar;2:286–297. [PMC free article] [PubMed] [Google Scholar]
- Gajl-Peczalska K. J., Bloomfield C. D., Coccia P. F., Sosin H., Brunning R. D., Kersey J. H. B and T cell lymphomas. Analysis of blood and lymph nodes in 87 patients. Am J Med. 1975 Nov;59(5):674–685. doi: 10.1016/0002-9343(75)90228-4. [DOI] [PubMed] [Google Scholar]
- Gearhart P. J., Sigal N. H., Klinman N. R. Production of antibodies of identical idiotype but diverse immunoglobulin classes by cells derived from a single stimulated B cell. Proc Natl Acad Sci U S A. 1975 May;72(5):1707–1711. doi: 10.1073/pnas.72.5.1707. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gmelig-Meyling F., van der Ham M., Ballieux R. E. The use of frozen-stored sheep erythrocytes for demonstrating lymphocytic membrane markers. J Immunol Methods. 1976;11(3-4):257–264. doi: 10.1016/0022-1759(76)90118-6. [DOI] [PubMed] [Google Scholar]
- Gordon I. L., Lukes R. J., O'Brien R. L., Parker J. W., Rembaum A., Russell R., Taylor C. R. Visualization of surface immunoglobulin of human B lymphocytes using microsophere-immunoglobulin conjugate in Giemsa-stained preparations. Clin Immunol Immunopathol. 1977 Jul;8(1):51–63. doi: 10.1016/0090-1229(77)90091-5. [DOI] [PubMed] [Google Scholar]
- Gupta S., Good R. A., Siegal F. P. Rosette-formation with mouse erythrocytes. II. A marker for human B and non-T lymphocytes. Clin Exp Immunol. 1976 Aug;25(2):319–327. [PMC free article] [PubMed] [Google Scholar]
- Hedfors E., Holm G., Ohnell B. Variations of blood lymphocytes during work studied by cell surface markers, DNA synthesis and cytotoxicity. Clin Exp Immunol. 1976 May;24(2):328–335. [PMC free article] [PubMed] [Google Scholar]
- Hiai H. Temperature-dependent rosette formation by mouse lymphoma cells as a result of viral hemadsorption. J Natl Cancer Inst. 1975 Oct;55(4):961–969. doi: 10.1093/jnci/55.4.961. [DOI] [PubMed] [Google Scholar]
- Hopper J. E. Comparative studies on monotypic IgM lambda and IgG kappa from an individual patient. IV. Immunofluorescent evidence for a common clonal synthesis. Blood. 1977 Aug;50(2):203–211. [PubMed] [Google Scholar]
- Horwitz D. A., Lobo P. I. Characterizaiton of two populations of human lymphocytes bearing easily detectable surface immunoglobulin. J Clin Invest. 1975 Dec;56(6):1464–1472. doi: 10.1172/JCI108227. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Jondal M., Holm G., Wigzell H. Surface markers on human T and B lymphocytes. I. A large population of lymphocytes forming nonimmune rosettes with sheep red blood cells. J Exp Med. 1972 Aug 1;136(2):207–215. doi: 10.1084/jem.136.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jondal M., Klein E., Yefenof E. Surface markers on human B and T lymphocytes. VII. Rosette formation between peripheral T lymphocytes and lymphoblastoid B-cell lines. Scand J Immunol. 1975;4(3):259–266. doi: 10.1111/j.1365-3083.1975.tb02625.x. [DOI] [PubMed] [Google Scholar]
- Kaplan J. Human T lymphocytes form rosettes with autologous and allogeneic human red blood cells. Clin Immunol Immunopathol. 1975 Mar;3(4):471–475. doi: 10.1016/0090-1229(75)90071-9. [DOI] [PubMed] [Google Scholar]
- Krueger G. R., Samii H., Sesterhenn K., Uhlmann C., Ablashi D. V., Fischer R., Wustrow F. Non-Hodgkin lymphomas: cell populations and functional behavior. Haematol Blood Transfus. 1977;20:55–60. doi: 10.1007/978-3-642-66639-1_6. [DOI] [PubMed] [Google Scholar]
- Kumagai K., Abo T., Sekizawa T., Sasaki M. Studies of surface immunoglobulins on human B lymphocytes. I. Dissociation of cell-bound immunoglobulins with acid pH or at 37 degrees C. J Immunol. 1975 Oct;115(4):982–987. [PubMed] [Google Scholar]
- Kunkel H. G. Surface markers of human lymphocytes. Johns Hopkins Med J. 1975 Nov;137(5):216–223. [PubMed] [Google Scholar]
- Kwok S. Y., Litwin S. D. Immunoglobulin expression of cells from human lymphoblastoid lines. III. Cell cycle phase and surface immunoglobulin expression. Cell Immunol. 1976 Aug;25(2):256–265. doi: 10.1016/0008-8749(76)90116-7. [DOI] [PubMed] [Google Scholar]
- Leech J. H., Glick A. D., Waldron J. A., Flexner J. M., Horn R. G., Collins R. D. Malignant lymphomas of follicular center cell origin in man. I. Immunologic studies. J Natl Cancer Inst. 1975 Jan;54(1):11–21. doi: 10.1093/jnci/54.1.11. [DOI] [PubMed] [Google Scholar]
- Leech J. H., Glick A. D., Waldron J. A., Flexner J. M., Horn R. G., Collins R. D. Malignant lymphomas of follicular center cell origin in man. I. Immunologic studies. J Natl Cancer Inst. 1975 Jan;54(1):11–21. doi: 10.1093/jnci/54.1.11. [DOI] [PubMed] [Google Scholar]
- Lennert K., Mestdagh J. Lymphogranulomatosen mit konstant hohem Epitheloidzellgehalt. Virchows Arch A Pathol Pathol Anat. 1968;344(1):1–20. [PubMed] [Google Scholar]
- Li C. Y., Yam L. T., Lam K. W. Acid phosphatase isoenzyme in human leukocytes in normal and pathologic conditions. J Histochem Cytochem. 1970 Jul;18(7):473–481. doi: 10.1177/18.7.473. [DOI] [PubMed] [Google Scholar]
- Litwin S. D., Lin P. K., Hütteroth T. H., Cleve H. Multiple heavy chains classes and light chain types on surfaces of cultured human lymphoid cells. Nat New Biol. 1973 Dec 12;246(154):179–181. doi: 10.1038/newbio246179a0. [DOI] [PubMed] [Google Scholar]
- Lobo P. I., Horwitz D. A. An appraisal of Fc receptors on human peripheral blood B and L lymphocytes. J Immunol. 1976 Sep;117(3):939–943. [PubMed] [Google Scholar]
- 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]
- Lukes R. J., Collins R. D. New approaches to the classification of the lymphomata. Br J Cancer Suppl. 1975 Mar;2:1–28. [PMC free article] [PubMed] [Google Scholar]
- Mason D. Y., Taylor C. R. The distribution of muramidase (lysozyme) in human tissues. J Clin Pathol. 1975 Feb;28(2):124–132. doi: 10.1136/jcp.28.2.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayer E. P., Teodorescu M., Reiter H., Dray S. Rabbit lymphocyte subpopulations. II. Separation and characterization of two Ig+ cell subpopulations. Cell Immunol. 1976 Mar 1;22(1):76–82. doi: 10.1016/0008-8749(76)90008-3. [DOI] [PubMed] [Google Scholar]
- Moretta L., Ferrarini M., Durante M. L., Mingari M. C. Expression of a receptor for IgM by human T cells in vitro. Eur J Immunol. 1975 Aug;5(8):565–569. doi: 10.1002/eji.1830050812. [DOI] [PubMed] [Google Scholar]
- Morse H. C., 3rd, Pumphrey J. G., Potter M., Asofsky R. Murine plasma cells secreting more than one class of immunoglobulin heavy chain. I. Frequency of two or more M-components in ascitic fluids from 788 primary plasmacytomas. J Immunol. 1976 Aug;117(2):541–547. [PubMed] [Google Scholar]
- Oriol R., Huerta J., Bouvet J. P., Liacopoulos P. Two myeloma globulins, IgG1-kappa and IgG1-lambda, from a single patient (Im). I. Purification and immunochemical characterization. Immunology. 1974 Dec;27(6):1081–1093. [PMC free article] [PubMed] [Google Scholar]
- Preud'Homme J. L., Seligmann M. Critical evaluation of B and T cell markers in man. Rheumatology. 1975;6:178–189. [PubMed] [Google Scholar]
- Preud'homme J. L., Labaume S. Immunofluorescent staining of human lymphocytes for the detection of surface immunoglobulins. Ann N Y Acad Sci. 1975 Jun 30;254:254–261. doi: 10.1111/j.1749-6632.1975.tb29175.x. [DOI] [PubMed] [Google Scholar]
- Rogers E. R., Parker J. W., Lukes R. J., D'Ablaing G., 3rd A simplified and modified methyl green pyronin stain. Am J Clin Pathol. 1970 Oct;54(4):667–669. doi: 10.1093/ajcp/54.4.667. [DOI] [PubMed] [Google Scholar]
- Ross G. D., Rabellino E. M., Polley M. J., Grey H. M. Combined studies of complement receptor and surface immunoglobulin-bearing cells and sheep erythrocyte rosette-forming cells in normal and leukemic human lymphocytes. J Clin Invest. 1973 Feb;52(2):377–385. doi: 10.1172/JCI107194. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rowlands D. T., Daniele R. P. Surface receptors in the immune response. N Engl J Med. 1975 Jul 3;293(1):26–32. doi: 10.1056/NEJM197507032930108. [DOI] [PubMed] [Google Scholar]
- Sen L., Mills B., Borella L. Erythrocyte receptors and thymus-associated antigens on human thymocytes, mitogen-induced blasts, and acute leukemia blasts. Cancer Res. 1976 Jul;36(7 Pt 1):2436–2441. [PubMed] [Google Scholar]
- Sheldon P. J., Holborow E. J. H-rosette formation in T-cell-proliferative diseases. Br Med J. 1975 Nov 15;4(5993):381–383. doi: 10.1136/bmj.4.5993.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shohat B., Joshua H. Formation of mouse red cell rosettes by lymphocytes from patients with chronic lymphatic leukemia and assessment of T cell function. Clin Immunol Immunopathol. 1976 Nov;6(3):389–393. doi: 10.1016/0090-1229(76)90092-1. [DOI] [PubMed] [Google Scholar]
- 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]
- Stathopoulos G., Elliott E. V. Formation of mouse or sheep red-blood-cell rosettes by lymphocytes from normal and leukaemic individuals. Lancet. 1974 Apr 6;1(7858):600–601. doi: 10.1016/s0140-6736(74)92655-5. [DOI] [PubMed] [Google Scholar]
- 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]
- Tak Yan Yu D. Lymphocyte subpopulations. Human red blood cell rosettes. Clin Exp Immunol. 1975 May;20(2):311–322. [PMC free article] [PubMed] [Google Scholar]
- Taylor C. R. An immunohistological study of follicular lymphoma, reticulum cell sarcoma and Hodgkin's disease. Eur J Cancer. 1976 Jan;12(1):61–75. doi: 10.1016/0014-2964(76)90125-0. [DOI] [PubMed] [Google Scholar]
- Taylor C. R. The nature of Reed-Sternberg cells and other malignant "reticulum" cells. Lancet. 1974 Oct 5;2(7884):802–807. doi: 10.1016/s0140-6736(74)91071-x. [DOI] [PubMed] [Google Scholar]
- Villiamey J., Bouvet J. P., Di Menza C., Boccara M. Myélome plasmocytaire "monoclonal" a deux paraprotéines, IgG kappa et IgG. Nouv Presse Med. 1974 Dec 28;3(45):2707–2711. [PubMed] [Google Scholar]
- Vitetta E. S., Forman J., Kettman J. R. Cell surface immunoglobulin. XVIII. Functional differences of B lymphocytes bearing different surface immunoglobulin isotypes. J Exp Med. 1976 May 1;143(5):1055–1065. doi: 10.1084/jem.143.5.1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Waldmann T. A., Broder S., Durm M., Blackman M., Krakauer R., Meade B. Suppressor T cells in the pathogenesis of hypogammaglobulinemia associated with a thymoma. Trans Assoc Am Physicians. 1975;88:120–134. [PubMed] [Google Scholar]
- Warner N. L. Membrane immunoglobulins and antigen receptors on B and T lymphocytes. Adv Immunol. 1974;19(0):67–216. doi: 10.1016/s0065-2776(08)60252-7. [DOI] [PubMed] [Google Scholar]
- Winchester R. J., Wernet P., Kunkel H. G., Dupont B., Jersild C., Fu S. M. Recognition by pregnancy serums of non-HL-A alloantigens selectively expressed on B lymphocytes. J Exp Med. 1975 Apr 1;141(4):924–929. [PMC free article] [PubMed] [Google Scholar]
- Wybran J., Fudenberg H. Editorial: How clinically useful is T and B cell quantitation? Ann Intern Med. 1974 Jun;80(6):765–767. doi: 10.7326/0003-4819-80-6-765. [DOI] [PubMed] [Google Scholar]
- Yam L. T., Li C. Y., Crosby W. H. Cytochemical identification of monocytes and granulocytes. Am J Clin Pathol. 1971 Mar;55(3):283–290. doi: 10.1093/ajcp/55.3.283. [DOI] [PubMed] [Google Scholar]
- van Rood J. J., van Leeuwen A., Termijtelen A., Keuning J. J. B-cell antibodies, Ia-like determinants, and their relation to MLC determinants in man. Transplant Rev. 1976;30:122–139. doi: 10.1111/j.1600-065x.1976.tb00218.x. [DOI] [PubMed] [Google Scholar]