Dasatinib Inhibits CXCR4 Signaling in Chronic Lymphocytic Leukaemia Cells and Impairs Migration Towards CXCL12

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  McCaig, Alison M ^a,c   Cosimo, Emilio ^a   Leach, Michael T ^b   Michie, Alison M ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b BEATSON WEST OF SCOTLAND CANCER CENTRE   (United Kingdom)

^c ROYAL ALEXANDRA HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; DASATINIB; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; STROMAL CELL DERIVED FACTOR 1;

ACTIN POLYMERIZATION; ADULT; AGED; ARTICLE; CELL COUNT; CELL STIMULATION; CHEMOTAXIS; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LEUKEMIA CELL; MALE; MIGRATION INHIBITION; PROTEIN EXPRESSION; STROMA CELL;

ACTINS; ADULT; AGED; ANIMALS; APOPTOSIS; CELL MOVEMENT; CHEMOKINE CXCL12; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; LIGANDS; MALE; MICE; MIDDLE AGED; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PYRIMIDINES; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; THIAZOLES;

MURINAE;

EID: 84868317373     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048929     Document Type: Article

References (35)

1. Burger JA, Ghia P, Rosenwald A, Caligaris-Cappio F, (2009) The microenvironment in mature B-cell malignancies: a target for new treatment strategies. Blood 114: 3367-3375.
2. Allen CD, Ansel KM, Low C, Lesley R, Tamamura H, et al. (2004) Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat Immunol 5: 943-952.
3. Burger JA, Burger M, Kipps TJ, (1999) Chronic lymphocytic leukaemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells. Blood 94: 3658-3667.
4. Burger JA, Tsukada N, Burger M, Zvaifler NJ, Dell'Aquila M, et al. (2000) Blood-derived nurse-like cells protect chronic lymphocytic leukaemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood 96: 2655-2663.
5. Ghia P, Chiorazzi N, Stamatopoulos K, (2008) Microenvironmental influences in chronic lymphocytic leukaemia: the role of antigen stimulation. J Intern Med 264: 549-562.
6. Lombardo LJ, Lee FY, Chen P, Norris D, Barrish JC, et al. (2004) Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxyethyl)- piperazin-1-yl)-2-methylpyrimidin-4- ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 47: 6658-6661.
7. Hantschel O, Rix U, Schmidt U, Burckstummer T, Kneidinger M, et al. (2007) The Btk tyrosine kinase is a major target of the Bcr-Abl inhibitor dasatinib. Proc Natl Acad Sci U S A 104: 13283-13288.
8. Hochhaus A, Kantarjian HM, Baccarani M, Lipton JH, Apperley JF, et al. (2007) Dasatinib induces notable hematologic and cytogenetic responses in chronic-phase chronic myeloid leukaemia after failure of imatinib therapy. Blood 109: 2303-2309.
9. McCaig AM, Cosimo E, Leach MT, Michie AM, (2011) Dasatinib inhibits B cell receptor signalling in chronic lymphocytic leukaemia but novel combination approaches are required to overcome additional pro-survival microenvironmental signals. Br J Haematol 153: 199-211.
10. Song Z, Lu P, Furman RR, Leonard JP, Martin P, et al. (2010) Activities of SYK and PLCgamma2 predict apoptotic response of CLL cells to SRC tyrosine kinase inhibitor dasatinib. Clin Cancer Res 16: 587-599.
11. Veldurthy A, Patz M, Hagist S, Pallasch CP, Wendtner CM, et al. (2008) The kinase inhibitor dasatinib induces apoptosis in chronic lymphocytic leukaemia cells in vitro with preference for a subgroup of patients with unmutated IgVH genes. Blood 112: 1443-1452.
12. Buettner R, Mesa T, Vultur A, Lee F, Jove R, (2008) Inhibition of Src family kinases with dasatinib blocks migration and invasion of human melanoma cells. Mol Cancer Res 6: 1766-1774.
13. Shor AC, Keschman EA, Lee FY, Muro-Cacho C, Letson GD, et al. (2007) Dasatinib inhibits migration and invasion in diverse human sarcoma cell lines and induces apoptosis in bone sarcoma cells dependent on SRC kinase for survival. Cancer Res 67: 2800-2808.
14. Serrels A, Macpherson IR, Evans TR, Lee FY, Clark EA, et al. (2006) Identification of potential biomarkers for measuring inhibition of Src kinase activity in colon cancer cells following treatment with dasatinib. Mol Cancer Ther 5: 3014-3022.
15. Bristol-Myers-Squibb (2006) Dasatinib (BMS-354825) Oncologic Drug Advisory Committee (ODAC) Briefing Document, NDA 21-986. Bristol-Myers-Squibb Company, Wallingford, CT USA. 21-986.
16. Hayden RE, Pratt G, Davies NJ, Khanim FL, Birtwistle J, et al. (2009) Treatment of primary CLL cells with bezafibrate and medroxyprogesterone acetate induces apoptosis and represses the pro-proliferative signal of CD40-ligand, in part through increased 15dDelta12,14,PGJ2. Leukaemia 23: 292-304.
17. Richardson SJ, Matthews C, Catherwood MA, Alexander HD, Carey BS, et al. (2006) ZAP-70 expression is associated with enhanced ability to respond to migratory and survival signals in B-cell chronic lymphocytic leukaemia (B-CLL). Blood 107: 3584-3592.
18. Burger M, Hartmann T, Krome M, Rawluk J, Tamamura H, et al. (2005) Small peptide inhibitors of the CXCR4 chemokine receptor (CD184) antagonize the activation, migration, and antiapoptotic responses of CXCL12 in chronic lymphocytic leukaemia B cells. Blood 106: 1824-1830.
19. Niedermeier M, Hennessy BT, Knight ZA, Henneberg M, Hu J, et al. (2009) Isoform-selective phosphoinositide 3'-kinase inhibitors inhibit CXCR4 signaling and overcome stromal cell-mediated drug resistance in chronic lymphocytic leukaemia: a novel therapeutic approach. Blood 113: 5549-5557.
20. O'Hayre M, Salanga CL, Kipps TJ, Messmer D, Dorrestein PC, et al. (2010) Elucidating the CXCL12/CXCR4 signaling network in chronic lymphocytic leukaemia through phosphoproteomics analysis. PLoS One 5: e11716.
21. Hoellenriegel J, Meadows SA, Sivina M, Wierda WG, Kantarjian H, et al. (2011) The phosphoinositide 3'-kinase delta inhibitor, CAL-101, inhibits B-cell receptor signaling and chemokine networks in chronic lymphocytic leukaemia. Blood 118: 3603-3612.
22. Ptasznik A, Urbanowska E, Chinta S, Costa MA, Katz BA, et al. (2002) Crosstalk between BCR/ABL oncoprotein and CXCR4 signaling through a Src family kinase in human leukaemia cells. J Exp Med 196: 667-678.
23. Nakata Y, Tomkowicz B, Gewirtz AM, Ptasznik A, (2006) Integrin inhibition through Lyn-dependent cross talk from CXCR4 chemokine receptors in normal human CD34+ marrow cells. Blood 107: 4234-4239.
24. Pleiman CM, Hertz WM, Cambier JC, (1994) Activation of phosphatidylinositol-3' kinase by Src-family kinase SH3 binding to the p85 subunit. Science 263: 1609-1612.
25. Buchner M, Baer C, Prinz G, Dierks C, Burger M, et al. (2010) Spleen tyrosine kinase inhibition prevents chemokine- and integrin-mediated stromal protective effects in chronic lymphocytic leukaemia. Blood 115: 4497-4506.
26. Quiroga MP, Balakrishnan K, Kurtova AV, Sivina M, Keating MJ, et al. (2009) B-cell antigen receptor signaling enhances chronic lymphocytic leukaemia cell migration and survival: specific targeting with a novel spleen tyrosine kinase inhibitor, R406. Blood 114: 1029-1037.
27. Braselmann S, Taylor V, Zhao H, Wang S, Sylvain C, et al. (2006) R406, an orally available spleen tyrosine kinase inhibitor blocks fc receptor signaling and reduces immune complex-mediated inflammation. J Pharmacol Exp Ther 319: 998-1008.
28. Hoellenriegel J, Coffey GP, Sinha U, Pandey A, Sivina M, et al. (2012) Selective, novel spleen tyrosine kinase (Syk) inhibitors suppress chronic lymphocytic leukaemia B-cell activation and migration. Leukaemia 26: 1576-1583.
29. de Rooij MF, Kuil A, Geest CR, Eldering E, Chang BY, et al. (2012) The clinically active BTK inhibitor PCI-32765 targets B-cell receptor- and chemokine-controlled adhesion and migration in chronic lymphocytic leukaemia. Blood 119: 2590-2594.
30. Ponader S, Chen SS, Buggy JJ, Balakrishnan K, Gandhi V, et al. (2012) Bruton's tyrosine kinase inhibitor PCI-32765 thwarts chronic lymphocytic leukaemia cell survival and tissue homing in vitro and in vivo. Blood 119: 1182-1189.
31. Lopez-Guerra M, Xargay-Torrent S, Perez-Galan P, Saborit-Villarroya I, Rosich L, et al. (2012) Sorafenib targets BCR kinases and blocks migratory and microenvironmental survival signals in CLL cells. Leukaemia 26: 1429-1432.
32. Friedberg JW, Sharman J, Sweetenham J, Johnston PB, Vose JM, et al. (2010) Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukaemia. Blood 115: 2578-2585.
33. Amrein PC, Attar EC, Takvorian T, Hochberg EP, Ballen KK, et al. (2011) Phase II study of dasatinib in relapsed or refractory chronic lymphocytic leukaemia. Clin Cancer Res 17: 2977-2986.
34. Willimott S, Baou M, Naresh K, Wagner SD, (2007) CD154 induces a switch in pro-survival Bcl-2 family members in chronic lymphocytic leukaemia. Br J Haematol 138: 721-732.
35. Hallaert DY, Jaspers A, van Noesel CJ, van Oers MH, Kater AP, et al. (2008) c-Abl kinase inhibitors overcome CD40-mediated drug resistance in CLL: implications for therapeutic targeting of chemoresistant niches. Blood 112: 5141-5149.