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PMID: 18551193 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Chronic lymphocytic leukemia T cells show impaired immunological synapse formation that can be reversed with an immunomodulating drug.

The Journal of clinical investigation ·Vol. 118 ·No. 7 ·2008-07-00 ·Pages 2427-37

Ramsay AG, Johnson AJ, Lee AM, Gorgün G, Le Dieu R, Blum W, Byrd JC, Gribben JG

Abstract

Cancer is associated with immune deficiency, but the biologic basis of this is poorly defined. Here we demonstrate that impaired actin polymerization results in CD4+ and CD8+ T cells from patients with chronic lymphocytic leukemia (CLL) exhibiting defective immunological synapse formation with APCs. Although this synapse dysfunction was in part a result of the CLL cells having poor APC function, defective actin polymerization was also identified in T cells from patients with CLL. We further demonstrate that, following contact with CLL cells, defects in immune synapse formation were induced in healthy allogeneic T cells. This required direct contact and was inhibited by blocking adhesion molecules on CLL B cells. In T cells from patients with CLL and in T cells from healthy individuals that had been in contact with CLL cells, recruitment of key regulatory proteins to the immune synapse was inhibited. Treatment of autologous T cells and CLL cells with the immunomodulating drug lenalidomide resulted in improved synapse formation. These results define what we believe to be a novel immune dysfunction in T cells from patients with CLL that has implications for both autologous and allogeneic immunotherapy approaches and identifies repair of immune synapse defects as an essential step in improving cancer immunotherapy approaches.

MeSH Terms
Actins/metabolism Animals Antigen Presentation/drug effects,immunology Antineoplastic Agents/pharmacology B-Lymphocytes/drug effects,immunology CD4-Positive T-Lymphocytes/drug effects,immunology,metabolism CD8-Positive T-Lymphocytes/drug effects,immunology,metabolism Humans Immunologic Factors/pharmacology Interleukin-2/metabolism Lenalidomide Leukemia, Lymphocytic, Chronic, B-Cell/blood,immunology Lymphocyte Activation/immunology Lymphocyte Culture Test, Mixed Lymphocyte Function-Associated Antigen-1/metabolism Lymphocyte Specific Protein Tyrosine Kinase p56(lck)/metabolism Mice Mice, Inbred Strains Mice, Transgenic Microfilament Proteins/metabolism Protein-Tyrosine Kinases/metabolism Proto-Oncogene Proteins/genetics Receptors, Antigen, T-Cell/metabolism Superantigens/immunology T-Lymphocytes/drug effects,immunology,metabolism T-Lymphocytes, Cytotoxic/immunology Thalidomide/analogs & derivatives,pharmacology
Chemicals
Actins Antineoplastic Agents Immunologic Factors Interleukin-2 Lymphocyte Function-Associated Antigen-1 Microfilament Proteins Proto-Oncogene Proteins Receptors, Antigen, T-Cell Superantigens Tcl1 protein, mouse Thalidomide Protein-Tyrosine Kinases Lymphocyte Specific Protein Tyrosine Kinase p56(lck) Lenalidomide
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Ramsay Alan G
Institute of Cancer, Centre for Medical Oncology, Barts and The London School of Medicine, University of London, London, United Kingdom.
Johnson Amy J
Lee Abigail M
Gorgün Güllü
Le Dieu Rifca
Blum William
Byrd John C
Gribben John G
References (45)
45 references, click to expand
  1. Enhancement of ligand-dependent activation of human natural killer T cells by lenalidomide: therapeutic implications.
    Blood. 2006 Jul 15;108(2):618-21 PMID: 16569772
  2. Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):6955-60 PMID: 12011454
  3. Lenalidomide induces complete and partial remissions in patients with relapsed and refractory chronic lymphocytic leukemia.
    Blood. 2008 Jun 1;111(11):5291-7 PMID: 18334676
  4. TCR, LFA-1, and CD28 play unique and complementary roles in signaling T cell cytoskeletal reorganization.
    J Immunol. 1999 Feb 1;162(3):1367-75 PMID: 9973391
  5. Lenalidomide for the treatment of B-cell malignancies.
    J Clin Oncol. 2008 Mar 20;26(9):1544-52 PMID: 18285605
  6. T-cell responses against chronic lymphocytic leukemia cells: implications for immunotherapy.
    Blood. 2002 Jul 1;100(1):167-73 PMID: 12070023
  7. Clinical efficacy of lenalidomide in patients with relapsed or refractory chronic lymphocytic leukemia: results of a phase II study.
    J Clin Oncol. 2006 Dec 1;24(34):5343-9 PMID: 17088571
  8. Identification of tumor-associated antigens in chronic lymphocytic leukemia by SEREX.
    Blood. 2002 Sep 15;100(6):2123-31 PMID: 12200376
  9. CD40-activated B-cell chronic lymphocytic leukemia cells for tumor immunotherapy: stimulation of allogeneic versus autologous T cells generates different types of effector cells.
    Blood. 1999 Mar 15;93(6):1992-2002 PMID: 10068672
  10. The immunological synapse: a molecular machine controlling T cell activation.
    Science. 1999 Jul 9;285(5425):221-7 PMID: 10398592
  11. Suppression of proximal T cell receptor signaling and lytic function in CD8+ tumor-infiltrating T cells.
    Cancer Res. 2007 Dec 1;67(23):11447-54 PMID: 18056473
  12. Human immunodeficiency virus type-1 infection impairs the formation of the immunological synapse.
    Immunity. 2006 May;24(5):547-61 PMID: 16713973
  13. Regulation of T-cell activation by the cytoskeleton.
    Nat Rev Immunol. 2007 Feb;7(2):131-43 PMID: 17259969
  14. Efficacy of lenalidomide in myelodysplastic syndromes.
    N Engl J Med. 2005 Feb 10;352(6):549-57 PMID: 15703420
  15. Reduced frequencies and suppressive function of CD4+CD25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine.
    Blood. 2005 Sep 15;106(6):2018-25 PMID: 15914560
  16. Follicular lymphomas can be induced to present alloantigen efficiently: a conceptual model to improve their tumor immunogenicity.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8200-4 PMID: 7545296
  17. Gene expression profiling of B cell chronic lymphocytic leukemia reveals a homogeneous phenotype related to memory B cells.
    J Exp Med. 2001 Dec 3;194(11):1625-38 PMID: 11733577
  18. Harnessing the immune system to treat cancer.
    J Clin Invest. 2007 May;117(5):1130-6 PMID: 17476342
  19. Higher doses of lenalidomide are associated with unacceptable toxicity including life-threatening tumor flare in patients with chronic lymphocytic leukemia.
    J Clin Oncol. 2008 May 20;26(15):2519-25 PMID: 18427150
  20. Cancer immunoediting: from immunosurveillance to tumor escape.
    Nat Immunol. 2002 Nov;3(11):991-8 PMID: 12407406
  21. Abnormal T-cell function in B-cell chronic lymphocytic leukaemia.
    Leuk Lymphoma. 2003 Mar;44(3):383-9 PMID: 12688308
  22. The immunological synapse: integrins take the stage.
    Immunol Rev. 2002 Aug;186:100-17 PMID: 12234366
  23. T-cell-antigen recognition and the immunological synapse.
    Nat Rev Immunol. 2003 Dec;3(12):973-83 PMID: 14647479
  24. Thalidomide costimulates primary human T lymphocytes, preferentially inducing proliferation, cytokine production, and cytotoxic responses in the CD8+ subset.
    J Exp Med. 1998 Jun 1;187(11):1885-92 PMID: 9607928
  25. Itk functions to control actin polymerization at the immune synapse through localized activation of Cdc42 and WASP.
    Curr Biol. 2003 Sep 16;13(18):1619-24 PMID: 13678593
  26. Modulation of the immunological synapse: a key to HIV-1 pathogenesis?
    Nat Rev Immunol. 2007 Apr;7(4):310-7 PMID: 17380160
  27. Transforming growth factor beta as endogenous growth inhibitor of chronic lymphocytic leukemia B cells.
    J Exp Med. 1994 Mar 1;179(3):999-1004 PMID: 8113691
  28. The role of the integrin LFA-1 in T-lymphocyte migration.
    Immunol Rev. 2007 Aug;218:135-46 PMID: 17624950
  29. A randomized phase 2 study of lenalidomide therapy for patients with relapsed or relapsed and refractory multiple myeloma.
    Blood. 2006 Nov 15;108(10):3458-64 PMID: 16840727
  30. Induction of cytotoxic T-cell responses against immunoglobulin V region-derived peptides modified at human leukocyte antigen-A2 binding residues.
    Blood. 2001 Nov 15;98(10):2999-3005 PMID: 11698283
  31. Immunoglobulin framework-derived peptides function as cytotoxic T-cell epitopes commonly expressed in B-cell malignancies.
    Nat Med. 2000 Jun;6(6):667-72 PMID: 10835683
  32. Chronic lymphocytic leukemia cells induce changes in gene expression of CD4 and CD8 T cells.
    J Clin Invest. 2005 Jul;115(7):1797-805 PMID: 15965501
  33. Wasp recruitment to the T cell:APC contact site occurs independently of Cdc42 activation.
    Immunity. 2001 Aug;15(2):249-59 PMID: 11520460
  34. T cell anergy and costimulation.
    Immunol Rev. 2003 Apr;192:161-80 PMID: 12670403
  35. Dynamin 2 regulates T cell activation by controlling actin polymerization at the immunological synapse.
    Nat Immunol. 2005 Mar;6(3):261-70 PMID: 15696170
  36. The three Es of cancer immunoediting.
    Annu Rev Immunol. 2004;22:329-60 PMID: 15032581
  37. Immune surveillance of tumors.
    J Clin Invest. 2007 May;117(5):1137-46 PMID: 17476343
  38. Acquired CD40-ligand deficiency in chronic lymphocytic leukemia.
    Nat Med. 1997 Sep;3(9):984-9 PMID: 9288724
  39. Defective proximal TCR signaling inhibits CD8+ tumor-infiltrating lymphocyte lytic function.
    J Immunol. 2005 Feb 15;174(4):1830-40 PMID: 15699109
  40. Autologous and allogeneic stem cell transplantations for poor-risk chronic lymphocytic leukemia.
    Blood. 2005 Dec 15;106(13):4389-96 PMID: 16131571
  41. Regulated expression of Mg2+ binding epitope on leukocyte integrin alpha subunits.
    EMBO J. 1989 Dec 1;8(12):3759-65 PMID: 2479549
  42. CD28 interaction with filamin-A controls lipid raft accumulation at the T-cell immunological synapse.
    Nat Cell Biol. 2006 Nov;8(11):1270-6 PMID: 17060905
  43. Activated T cells induce expression of B7/BB1 on normal or leukemic B cells through a CD40-dependent signal.
    J Exp Med. 1993 Apr 1;177(4):925-35 PMID: 7681471
  44. Characterization of the TCL-1 transgenic mouse as a preclinical drug development tool for human chronic lymphocytic leukemia.
    Blood. 2006 Aug 15;108(4):1334-8 PMID: 16670263
  45. Interleukin-6 and interleukin-10 levels in chronic lymphocytic leukemia: correlation with phenotypic characteristics and outcome.
    Blood. 2001 Jan 1;97(1):256-63 PMID: 11133769
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2008-07-00
Pages
2427-37
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC2423865
Subset
IM
Grants
NCI NIH HHS · P01 CA095426 · United States
NCI NIH HHS · P01 CA95426 · United States
NCI NIH HHS · P01 CA81538 · United States
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