Leukemia Research
Volume 24, Issue 7 , Pages 611-621 , July 2000

Disruption of the IFN-γ cytokine network in chronic lymphocytic leukemia contributes to resistance of leukemic B cells to apoptosis

  • Mohamed Zaki

      Affiliations

    • Department of Pathology and Laboratory Medicine, School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6082, USA
    • Ain Shams University, Cairo, Egypt
  • ,
  • Raymond Douglas

      Affiliations

    • Department of Pathology and Laboratory Medicine, School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6082, USA
  • ,
  • Nancy Patten

      Affiliations

    • Department of Pathology and Laboratory Medicine, School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6082, USA
  • ,
  • Margaret Bachinsky

      Affiliations

    • Department of Pathology and Laboratory Medicine, School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6082, USA
  • ,
  • Roberta Lamb

      Affiliations

    • Department of Pathology and Laboratory Medicine, School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6082, USA
  • ,
  • Peter Nowell

      Affiliations

    • Department of Pathology and Laboratory Medicine, School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6082, USA
  • ,
  • Jonni Moore

      Affiliations

    • Department of Pathology and Laboratory Medicine, School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6082, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1-215-8986853; fax: +1-215-8984227

Received 12 August 1999 ,Accepted 27 January 2000.

References 

  1. Dighiero G, Travade P, Chevret S, et al.  B-cell chronic lymphocytic leukemia: present status and future directions. French cooperative group on CLL. Blood. 1901;78:1991
  2. Cheson B, Bennett J, Grever M, et al.  National Cancer institute-sponsored working group guidelines for chronic lymphocytic leukemia: revised guidelines for diagnosis and treatment. Blood. 1996;87:4990
  3. Agular-Santelises M, Rottenberg ME, Lewin N, Mellstedt H, Jondal M. Bcl-2, Bax and p53 expression in B-CLL in relation to in vitro survival and clinical progression. Int. J. Cancer. 1996;69:114
  4. Caligaris-Cappio F, Gottardi D, Alfarano A, et al.  The nature of the B lymphocyte in B-chronic lymphocytic leukemia. Blood Cells. 1993;19:601
  5. Dighiero G. Biology of the neoplastic lymphocyte in BCLL baillieres. Clin. Haematol. 1993;6:807
  6. Foon KA. Chronic lymphoid leukemias: recent advances in biology and therapy. Stem Cells. 1995;13:1
  7. Schuler M, Huber C, Peschel C. Cytokines in the pathophysiology and treatment of chronic B-cell malignancies: a review. Annal. Hematol. 1995;71:57
  8. Hernandez JM, Mecucci C, Criel A, et al.  Cytogenetic analysis of B cell chronic lymphoid leukemias classified according to morphologic and immunophenotypic (FAB) criteria. Leukemia. 1995;9:2140
  9. Mould S, Gardiner A, Corcoran M, Oscier DG. Trisomy 12 and structural abnormalities of 13q14 occurring in the same clone in chronic lymphocytic leukaemia. Br. J. Haematol. 1996;92:389
  10. Gahrton G, Juliusson G, Robert KH, Friberg K. Role of chromosomal abnormalities in chronic lymphocytic leukemia. Blood Rev. 1987;1:183
  11. Escudier SM, Pereira-Leahy JM, Drach JW, et al.  Fluorescent in situ hybridization and cytogenetic studies of trisomy 12 in chronic lymphocytic leukemia. Blood. 1993;81:2702
  12. Raghoebier S, van Krieken JH, Kluin-Nelemans , et al.  Oncogene rearrangements in chronic B-cell leukemia. Blood. 1991;77:1560
  13. Dighiero G. An attempt to explain disordered immunity and hypogammaglobulinemia in CLL. Nouv. Rev. Fr. Hematol. 1988;30:283
  14. Chapel H, Buch C. Mechanisms of infection in chronic lymphocytic leukemia. Semin. Hematol. 1987;24:291
  15. Swain SL, Bradley LM, Croft M, et al.  Helper T cells subsets: phenotype function and role of lymphokines in regulating their development. Immunol. Rev. 1991;123:115
  16. Douglas R, Capocasale R, Lamb R, Nowell P, Moore J. CLL B cells are resistant to the apoptotic effects of transforming growth factor-beta (TGF-β). Blood. 1997;89:941
  17. Dancescu M, Rubio-Trujillo M, Biron G, et al.  Interleukin 4 protects chronic lymphocytic leukemic B cells from death by apoptosis and upregulates Bcl-2 expression. J. Exp. Med. 1992;176:1319
  18. Panayiotidis P, Ganeshaguru K, Jabbar SA, Hoffbrand AV. Interleukin-4 inhibits apoptotic cell death and loss of the bcl-2 protein in B-chronic lymphocytic leukaemia cells in vitro. Br. J. Haematol. 1993;85:439
  19. Pace J, Russell S, Torres B, Johnson H, Gray P. Recombinant mouse gamma interferon induces the priming step in macrophage activation for tumor cell killing. J. Immunol. 1983;130:2011
  20. Paul W. Fundamental Immunology. Third Edition. New York: Raven Press, Ltd; 1993;
  21. Trinchieri G, Perussia B. Immune interferon: a pleiotropic lymphokine with multiple effects. Immunol. Today. 1985;6:131
  22. Defrance T, Vanbervliet B, Aubry JP, et al.  B cell growth-promoting activity of recombinant human interleukin 4. J. Immunol. 1987;139:1135
  23. Karray S, Vazquez A, Merle-Beral H, et al.  Synergistic effect of recombinant IL 2 and interferon-gamma on the proliferation of human monoclonal lymphocytes. J. Immunol. 1987;138:3824
  24. Mu Xi, Kay NE, Gosland MP, Jennings CD. Analysis of blood T-cell cytokine expression in B-chronic lymphocytic leukaemia: evidence for increased levels of cytoplasmic IL-4 in resting and activated CD8 T cells. Br. J. Haematol. 1997;96(4):733
  25. Mainou-Fowler T, Copplestone JA, Prentice AG. Effect of interleukins on the proliferation and survival of B cell chronic lymphocytic leukaemia cells. J. Clin. Pathol. 1995;48:482
  26. Rojas R, Roman J, Torres A, et al.  Inhibition of apoptotic cell death in B-CLL by Interferon gamma correlates with clinical stage. Leukemia. 1996;10(11):1782–1788
  27. Zaki MH, Douglas RS, Patten N, et al.  Resistance of CLL B cells to apoptosis: Involvement of type 1 (interferon-gamma) cytokine pathways. Blood. 1998;92:4177
  28. Buschle M, Campana D, Carding SR, et al.  Interferon gamma inhibits apoptotic cell death in B cell chronic lymphocytic leukemia. J. Exp. Med. 1993;177:213
  29. Reyes E, Prieto A, Carrion F, et al.  Altered pattern of cytokine production by peripheral blood CD2+ cells from B chronic lymphocytic leukemia patients. Am. J. Hematol. 1998;57:93
  30. Gorczyca W, Gong J, Darzynkiewicz Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 1945;53:1993
  31. Hotz MA, Gong J, Traganos F, Darzynkiewicz Z. Flow cytometric detection of apoptosis: comparison of the assays of in situ DNA degradation and chromatin changes. Cytometry. 1994;15:237
  32. Telford WG, King LE, Fraker PJ. Comparative evaluation of several DNA binding dyes in the detection of apoptosis-associated chromatin degradation by flow cytometry. Cytometry. 1992;13:137
  33. Jung T, Schauer U, Heusser C, Neumann C, Reiger C. Detection of intracellular cytokines by flow cytometry. J. Immunol. Methods. 1993;159:197
  34. Freedman AS. Immunobiology of chronic lymphocytic leukemia. Hematol.–Oncol. Clin. North Am. 1990;4:405
  35. Moore JS, Friedman DF, Silberstein LE, Besa EC, Nowell PC. Clinical heterogeneity reflects biologic diversity in chronic lymphocytic leukemia. Crit. Rev. Oncol.–Hematol. 1995;20:141
  36. Montserrat E, Rozman C. Chronic lymphocytic leukemia: present status. Annal. Oncol. 1995;6:219
  37. Jewell AP, Lydyard PM, Worman CP, Giles FJ, Goldstone AH. Growth factors can protect B-chronic lymphocytic leukemia cells against programmed cell death without stimulating proliferation. Leuk. Lymph. 1995;18:159
  38. O'Brien S, del Giglio A, Keating M. Advances in the biology and treatment of B-cell chronic lymphocytic leukemia. Blood. 1995;85:307
  39. Molica S, De Rossi G, Luciani M, Levato D. Prognostic features and therapeutical approaches in B-cell chronic lymphocytic leukemia: an update. Haematologica. 1995;80:176
  40. Pestka S. The interferon receptors. Semin. Oncol. 1997;9:S9
  41. Decker T, Flohr T, Trautmann P, et al.  Role of accessory cells in cytokine production by T cells in chronic B-cell lymphocytic leukemia. Blood. 1995;86:1115
  42. Mosmann T, Sad S. The expanding universe of T cell subsets: Th1, Th2 and more. Immunol. Today. 1996;17:138
  43. Ulloa L, Doody J, Massague J. Inhibition of transforming growth factor-β/SMAD signalling by the interferon-γ/STAT pathway. Nature. 1999;397:710
  44. Fournier S, Rubio M, Delespesse G, Sarfati M. Role for low-affinity receptor for IgE (CD23) in normal and leukemic B-cell proliferation. Blood. 1881;84:1994
  45. Fournier S, Yang L, Delespesse G, et al.  The two CD23 isoforms display differential regulation in chronic lymphocytic leukemia. Br. J. Haematol. 1995;89:373
  46. Holder MJ, Liu YJ, Defrance T, et al.  Growth factor requirements for the stimulation of germinal center B cells: evidence for an IL-2-dependent pathway of development. Int. Immunol. 1991;3:1243
  47. Douglas RS, Woo EY, Capocasale RJ, et al.  Altered response to and production of TGF-b by cells from Autoimmune NZB mice. Cell Immunol. 1997;179:129

 Supported in part by National Institutes of Health grant CA42232 and the Lucille P. Markey Charitable Trust.

PII: S0145-2126(00)00022-9

Leukemia Research
Volume 24, Issue 7 , Pages 611-621 , July 2000