Lenalidomide reduces survival of chronic lymphocytic leukemia cells in primary cocultures by altering the myeloid microenvironment

Blood

Volumn 121, Issue 13, 2013, Pages 2503-2511

  Schulz, Angela ^a   Dürr, Claudia ^a   Zenz, Thorsten ^b,c   Döhner, Hartmut ^c   Stilgenbauer, Stephan ^c   Lichter, Peter ^a   Seiffert, Martina ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; LENALIDOMIDE; STAT1 PROTEIN; ANTINEOPLASTIC AGENT; DRUG DERIVATIVE; THALIDOMIDE;

ADULT; AGED; ARTICLE; CELL MIGRATION; CELL SURFACE; CHEMOTAXIS ASSAY; CHRONIC LYMPHATIC LEUKEMIA; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; FLOW CYTOMETRY; HUMAN; IMMUNOBLOTTING; IMMUNOPHENOTYPING; IN VITRO STUDY; LEUKEMIA CELL; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; THERAPY EFFECT; TUMOR MICROENVIRONMENT; BONE MARROW; BONE MARROW CELL; CELL SURVIVAL; DRUG EFFECT; DRUG SCREENING; PATHOLOGY; PRIMARY CELL CULTURE; TUMOR CELL CULTURE;

ADULT; AGED; ANTINEOPLASTIC AGENTS; BONE MARROW; CELL SURVIVAL; COCULTURE TECHNIQUES; DRUG EVALUATION, PRECLINICAL; FEMALE; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MIDDLE AGED; MYELOID CELLS; PRIMARY CELL CULTURE; THALIDOMIDE; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

MLCS; MLOWN;

EID: 84878411869     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-08-447664     Document Type: Article

References (40)

1. Dores GM, Anderson WF, Curtis RE, et al. Chronic lymphocytic leukaemia and small lymphocytic lymphoma: overview of the descriptive epidemiology. Br J Haematol. 2007;139(5): 809-819.
2. Lagneaux L, Delforge A, Bron D, et al. Chronic lymphocytic leukemic B cells but not normal B cells are rescued from apoptosis by contact with normal bone marrow stromal cells. Blood. 1998; 91(7):2387-2396.
3. Tsukada N, Burger JA, Zvaifler NJ, et al. Distinctive features of “nurselike” cells that differentiate in the context of chronic lymphocytic leukemia. Blood. 2002;99(3):1030-1037.
4. Burger JA, Tsukada N, Burger M, et al. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood. 2000;96(8):2655-2663.
5. Deaglio S, Vaisitti T, Bergui L, et al. CD38 and CD100 lead a network of surface receptors relaying positive signals for B-CLL growth and survival. Blood. 2005;105(8):3042-3050.
6. Ysebaert L, Fournié JJ. Genomic and phenotypic characterization of nurse-like cells that promote drug resistance in chronic lymphocytic leukemia. Leuk Lymphoma. 2011;52(7):1404-1406.
7. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009; 9(4):239-252.
8. Seiffert M, Schulz A, Ohl S, et al. Soluble CD14 is a novel monocyte-derived survival factor for chronic lymphocytic leukemia cells, which is induced by CLL cells in vitro and present at abnormally high levels in vivo. Blood. 2010; 116(20):4223-4230.
9. Schulz A, Toedt G, Zenz T, et al. Inflammatory cytokines and signaling pathways are associated with survival of primary chronic lymphocytic leukemia cells in vitro: a dominant role of CCL2. Haematologica. 2011;96(3):408-416.
10. Chanan-Khan AA, Cheson BD. Lenalidomide for the treatment of B-cell malignancies. J Clin Oncol. 2008;26(9):1544-1552.
11. Badoux XC, Keating MJ, Wen S, et al. Lenalidomide as initial therapy of elderly patients with chronic lymphocytic leukemia. Blood. 2011; 118(13):3489-3498.
12. Ferrajoli A, Lee BN, Schlette EJ, et al. Lenalidomide induces complete and partial remissions in patients with relapsed and refractory chronic lymphocytic leukemia. Blood. 2008; 111(11):5291-5297.
13. Wendtner C-M, Hillmen P, Mahadevan D, et al. Final results of a multicenter phase 1 study of lenalidomide in patients with relapsed or refractory chronic lymphocytic leukemia. Leuk Lymphoma. 2012;53(3):417-423.
14. Chanan-Khan AA, Chitta K, Ersing N, et al. Biological effects and clinical significance of lenalidomide-induced tumour flare reaction in patients with chronic lymphocytic leukaemia: in vivo evidence of immune activation and antitumour response. Br J Haematol. 2011; 155(4):457-467.
15. Lee B-N, Gao H, Cohen EN, et al. Treatment with lenalidomide modulates T-cell immunophenotype and cytokine production in patients with chronic lymphocytic leukemia. Cancer. 2011;117(17): 3999-4008.
16. Lapalombella R, Andritsos L, Liu Q, et al. Lenalidomide treatment promotes CD154 expression on CLL cells and enhances production of antibodies by normal B cells through a PI3-kinase-dependent pathway. Blood. 2010;115(13): 2619-2629.
17. Ramsay AG, Johnson AJ, Lee AM, et al. Chronic lymphocytic leukemia T cells show impaired immunological synapse formation that can be reversed with an immunomodulating drug. J Clin Invest. 2008;118(7):2427-2437.
18. Gorgun G, Ramsay AG, Holderried TAW, et al. E(m)-TCL1 mice represent a model for immunotherapeutic reversal of chronic lymphocytic leukemia-induced T-cell dysfunction. Proc Natl Acad Sci USA. 2009;106(15):6250-6255.
19. Xu Y, Li J, Ferguson GD, et al. Immunomodulatory drugs reorganize cytoskeleton by modulating Rho GTPases. Blood. 2009;114(2):338-345.
20. Liang X, Moseman EA, Farrar MA, et al. Toll-like receptor 9 signaling by CpG-B oligodeoxynucleotides induces an apoptotic pathway in human chronic lymphocytic leukemia B cells. Blood. 2010;115(24):5041-5052.
21. Walter MJ, Look DC, Tidwell RM, et al. Targeted inhibition of interferon-gamma-dependent intercellular adhesion molecule-1 (ICAM-1) expression using dominant-negative Stat1. J Biol Chem. 1997;272(45):28582-28589.
22. Batista FD, Iber D, Neuberger MS. B cells acquire antigen from target cells after synapse formation. Nature. 2001;411(6836):489-494.
23. Giannopoulos K, Mertens D, Stilgenbauer S. Treating chronic lymphocytic leukemia with thalidomide and lenalidomide. Expert Opin Pharmacother. 2011;12(18):2857-2864.
24. Bhattacharya N, Diener S, Idler IS, et al. Nurselike cells show deregulated expression of genes involved in immunocompetence. Br J Haematol. 2011;154(3):349-356.
25. Chanan-Khan A, Miller KC, Musial L, et al. Clinical efficacy of lenalidomide in patients with relapsed or refractory chronic lymphocytic leukemia: results of a phase II study. J Clin Oncol. 2006;24(34): 5343-5349.
26. Kröber A, Seiler T, Benner A, et al. V(H) mutation status, CD38 expression level, genomic aberrations, and survival in chronic lymphocytic leukemia. Blood. 2002;100(4):1410-1416.
27. Döhner H, Stilgenbauer S, Benner A, et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med. 2000; 343(26):1910-1916.
28. Nishio M, Endo T, Tsukada N, et al. Nurselike cells express BAFF and APRIL, which can promote survival of chronic lymphocytic leukemia cells via a paracrine pathway distinct from that of SDF-1alpha. Blood. 2005;106(3):1012-1020.
29. Roca H, Varsos ZS, Sud S, et al. CCL2 and interleukin-6 promote survival of human CD11b1 peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem. 2009;284(49):34342-34354.
30. Tanikawa T, Wilke CM, Kryczek I, et al. Interleukin-10 ablation promotes tumor development, growth, and metastasis. Cancer Res. 2012;72(2):420-429.
31. Koppelman B, Neefjes JJ, de Vries JE, et al. Interleukin-10 down-regulates MHC class II alphabeta peptide complexes at the plasma membrane of monocytes by affecting arrival and recycling. Immunity. 1997;7(6):861-871.
32. Wanidworanun C, Strober W. Predominant role of tumor necrosis factor-alpha in human monocyte IL-10 synthesis. J Immunol. 1993;151(12): 6853-6861.
33. Kamiguti AS, Lee ES, Till KJ, et al. The role of matrix metalloproteinase 9 in the pathogenesis of chronic lymphocytic leukaemia. Br J Haematol. 2004;125(2):128-140.
34. Redondo-Muñoz J, Ugarte-Berzal E, Terol MJ, et al. Matrix metalloproteinase-9 promotes chronic lymphocytic leukemia b cell survival through its hemopexin domain. Cancer Cell. 2010;17(2): 160-172.
35. Ugarte-Berzal E, Redondo-Muñoz J, Eroles P, et al. VEGF/VEGFR2 interaction down-regulates matrix metalloproteinase-9 via STAT1 activation and inhibits B chronic lymphocytic leukemia cell migration. Blood. 2010;115(4):846-849.
36. Baran-Marszak F, Feuillard J, Najjar I, et al. Differential roles of STAT1alpha and STAT1beta in fludarabine-induced cell cycle arrest and apoptosis in human B cells. Blood. 2004;104(8): 2475-2483.
37. Riches JC, Sangaralingam A, Kiaii S, et al. Impact of lenalidomide on gene expression profiles of malignant and immune cells in patients with chronic lymphocytic leukemia. [published online ahead of print January 24, 2013]. Blood.
38. Vega FM, Fruhwirth G, Ng T, et al. RhoA and RhoC have distinct roles in migration and invasion by acting through different targets. J Cell Biol. 2011;193(4):655-665.
39. Cai L, Marshall TW, Uetrecht AC, et al. Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell. 2007;128(5): 915-929.
40. Troeger A, Johnson AJ, Wood J, et al. RhoH is critical for cell-microenvironment interactions in chronic lymphocytic leukemia in mice and humans. Blood. 2012;119(20):4708-4718.