Treatment with ibrutinib inhibits BTK- and VLA-4-dependent adhesion of chronic lymphocytic leukemia cells in vivo

Clinical Cancer Research

Volumn 21, Issue 20, 2015, Pages 4642-4651

  Herman, Sarah E M ^a   Mustafa, Rashida Z ^a   Jones, Jade ^a,b   Wong, Deanna H ^a   Farooqui, Mohammed ^a   Wiestner, Adrian ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN; BETA1 INTEGRIN; BRUTON TYROSINE KINASE; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR4; FIBRONECTIN; FIRATEGRAST; HERMES ANTIGEN; IBRUTINIB; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; PROTEIN KINASE C; STROMAL CELL DERIVED FACTOR 1; VERY LATE ACTIVATION ANTIGEN 4; AGAMMAGLOBULINAEMIA TYROSINE KINASE; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ARTICLE; BONE MARROW STROMA CELL; CANCER INHIBITION; CELL ADHESION; CELL MIGRATION; CELL STIMULATION; CELL SURFACE; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; ENZYME ACTIVATION; EX VIVO STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; LYMPHOCYTOSIS; MAJOR CLINICAL STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; AGED; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; FEMALE; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; METABOLISM;

AGED; CELL ADHESION; FEMALE; FIBRONECTINS; HUMANS; INTEGRIN ALPHA4BETA1; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOCYTOSIS; MALE; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PYRAZOLES; PYRIMIDINES;

EID: 84945561515     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-0781     Document Type: Article

References (50)

1. Caligaris-Cappio F, Ghia P. Novel insights in chronic lymphocytic leukemia: are we getting closer to understanding the pathogenesis of the disease? J Clin Oncol 2008;26:4497-503.
2. Duhren-von Minden M, Ubelhart R, Schneider D, Wossning T, Bach MP, Buchner M, et al. Chronic lymphocytic leukaemia is driven by antigen-independent cell-autonomous signalling. Nature 2012;489: 309-12.
3. Burger JA, Ghia P, Rosenwald A, Caligaris-Cappio F. The microenvironment in mature B-cell malignancies: a target for new treatment strategies. Blood 2009;114:3367-75.
4. Herishanu Y, Perez-Galan P, Liu D, Biancotto A, Pittaluga S, Vire B, et al. The lymph node microenvironment promotes B-cell receptor signaling, NF-kappaB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood 2011;117:563-74.
5. Dal Bo M, Tissino E, Benedetti D, Caldana C, Bomben R, Del Poeta G, et al. Microenvironmental interactions in chronic lymphocytic leukemia: the master role of CD49d. Semin Hematol 2014;51:168-76.
6. Stevenson FK, Forconi F, Packham G. The meaning and relevance of B-cell receptor structure and function in chronic lymphocytic leukemia. Semin Hematol 2014;51:158-67.
7. Wiestner A. Emerging role of kinase-targeted strategies in chronic lympho-cytic leukemia. Blood 2012;120:4684-91.
8. Burger JA, Chiorazzi N. B cell receptor signaling in chronic lymphocytic leukemia. Trends Immunol 2013;34:592-601.
9. Humphries LA, Dangelmaier C, Sommer K, Kipp K, Kato RM, Griffith N, et al. Tec kinases mediate sustained calcium influx via site-specific tyrosine phosphorylation of the phospholipase Cgamma Src homology 2-Src homology 3 linker. J Biol Chem 2004;279:37651-61.
10. Kil LP, de Bruijn MJ, van Hulst JA, Langerak AW, Yuvaraj S, Hendriks RW. Bruton's tyrosine kinase mediated signaling enhances leukemogenesis in a mouse model for chronic lymphocytic leukemia. Am J Blood Res 2013; 3:71-83.
11. Woyach JA, Bojnik E, Ruppert AS, Stefanovski MR, Goettl VM, Smucker KA, et al. Bruton's tyrosine kinase (BTK) function is important to the development and expansion of chronic lymphocytic leukemia (CLL). Blood 2014;123:1207-13.
12. Advani RH, Buggy JJ, Sharman JP, Smith SM, Boyd TE, Grant B, et al. Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765) has significant activity in patients with relapsed/refractory B-cell malignancies. J Clin Oncol 2013; 31:88-94.
13. Byrd JC, Furman RR, Coutre SE, Flinn IW, Burger JA, Blum KA, et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N Engl J Med 2013;369:32-42.
14. Farooqui MZ, Valdez J, Martyr S, Aue G, Saba N, Niemann CU, et al. Ibrutinib for previously untreated and relapsed or refractory chronic lymphocytic leukaemia with TP53 aberrations: a phase 2, single-arm trial. Lancet Oncol 2014;16:169-176.
15. Byrd JC, Brown JR, O'Brien S, Barrientos JC, Kay NE, Reddy NM, et al. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N Engl J Med 2014;371:213-23.
16. Herman SE, Niemann CU, Farooqui M, Jones J, Mustafa RZ, Lipsky A, et al. Ibrutinib-induced lymphocytosis in patients with chronic lymphocytic leukemia: correlative analyses from a phase II study. Leukemia 2014;28: 2188-96.
17. Herishanu Y, Katz BZ, Lipsky A, WiestnerA.Biologyofchronic lymphocytic leukemia in different microenvironments: clinical and therapeutic implications. Hematol Oncol Clin North Am 2013;27:173-206.
18. de Rooij MF, Kuil A, Geest CR, Eldering E, Chang BY, Buggy JJ, et al. The clinically active BTK inhibitor PCI-32765 targets B-cell receptor-and chemokine-controlled adhesion and migration in chronic lymphocytic leukemia. Blood 2012;119:2590-4.
19. Ponader S, Chen SS, Buggy JJ, Balakrishnan K, Gandhi V, Wierda WG, et al. The Bruton tyrosine kinase inhibitor PCI-32765 thwarts chronic lympho-cytic leukemia cell survival and tissue homing in vitro and in vivo. Blood 2012;119:1182-9.
20. DalBo M, Bomben R, Zucchetto A, Del Poeta G, Gaidano G, Deaglio S, et al. Microenvironmental interactions in chronic lymphocytic leukemia: hints for pathogenesis and identification of targets for rational therapy. Curr Pharm Des 2012;18:3323-34.
21. Zucchetto A, Vaisitti T, Benedetti D, Tissino E, Bertagnolo V, Rossi D, et al. The CD49d/CD29 complex is physically and functionally associated with CD38 in B-cell chronic lymphocytic leukemia cells. Leukemia 2012;26: 1301-12.
22. Bulian P, Shanafelt TD, Fegan C, Zucchetto A, Cro L, Nuckel H, et al. CD49d Is the strongest flow cytometry-based predictor of overall survival in chronic lymphocytic leukemia. J Clin Oncol 2014;32:897-904.
23. Pepper C, Buggins AG, Jones CH, Walsby EJ, Forconi F, Pratt G, et al. Phenotypic heterogeneity in IGHV-mutated CLL patients has prognostic impact and identifies a subset with increased sensitivity to BTK and PI3Kdelta inhibition. Leukemia 2015;29:744-7.
24. Burger M, Hartmann T, Krome M, Rawluk J, Tamamura H, Fujii N, et al. Small peptide inhibitors of the CXCR4 chemokine receptor (CD184) antagonize the activation, migration, and antiapoptotic responses of CXCL12 in chronic lymphocytic leukemia B cells. Blood 2005;106: 1824-30.
25. Herman SE, Sun X, McAuley EM, Hsieh MM, Pittaluga S, Raffeld M, et al. Modeling tumor-host interactions of chronic lymphocytic leukemia in xenografted mice to study tumor biology and evaluate targeted therapy. Leukemia 2013;27:1769-73.
26. Herman SE, Barr PM, McAuley EM, Liu D, Wiestner A, Friedberg JW. Fostamatinib inhibits B-cell receptor signaling, cellular activation and tumor proliferation in patients with relapsed and refractory chronic lym-phocytic leukemia. Leukemia 2013;27:1769-73.
27. Jalkanen S, Jalkanen M. Lymphocyte CD44 binds the COOH-terminal heparin-binding domain of fibronectin. J Cell Biol 1992;116:817-25.
28. To WS, Midwood KS. Plasma and cellular fibronectin: distinct and independent functions during tissue repair. Fibrogenesis Tissue Repair 2011; 4:21.
29. Spaargaren M, Beuling EA, Rurup ML, Meijer HP, Klok MD, Middendorp S, et al. The B cell antigen receptor controls integrin activity through Btk and PLCgamma2. J Exp Med 2003;198:1539-50.
30. de Gorter DJ, Beuling EA, Kersseboom R, Middendorp S, van Gils JM, Hendriks RW, et al. Bruton's tyrosine kinase and phospholipase Cgamma2 mediate chemokine-controlled B cell migration and homing. Immunity 2007;26:93-104.
31. Hurley JH, Newton AC, Parker PJ, Blumberg PM, Nishizuka Y. Taxonomy and function of C1 protein kinase C homology domains. Protein Sci 1997;6:477-80.
32. Friedberg JW, Sharman J, Sweetenham J, Johnston PB, Vose JM, Lacasce A, et al. Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia. Blood 2010;115:2578-85.
33. Herman SE, Gordon AL, Hertlein E, Ramanunni A, Zhang X, Jaglowski S, et al. Bruton tyrosine kinase represents a promising therapeutic target for treatment of chronic lymphocytic leukemia and is effectively targeted by PCI-32765. Blood 2011;117:6287-96.
34. Srichai M, Zent R. Integrin structure and function. In:Zent R, Pozzi A, editors. Cell-extracellular matrix interactions in cancer: Springer New York, NY; 2010. p. 19-41.
35. Arana E, Harwood NE, Batista FD. Regulation of integrin activation through the B-cell receptor. J Cell Sci 2008;121:2279-86.
36. Calissano C, Damle RN, Marsilio S, Yan XJ, Yancopoulos S, Hayes G, et al. Intraclonal complexity in chronic lymphocytic leukemia: fractions enriched in recently born/divided and older/quiescent cells. Mol Med 2011;17:1374-82.
37. Walsby E, Buggins A, Devereux S, Jones C, Pratt G, Brennan P, et al. Development and characterization of a physiologically relevant model of lymphocyte migration in chronic lymphocytic leukemia. Blood 2014;123: 3607-17.
38. de la Fuente MT, Casanova B, Garcia-Gila M, Silva A, Garcia-Pardo A. Fibronectin interaction with alpha4beta1 integrin prevents apoptosis in B cell chronic lymphocytic leukemia: correlation with Bcl-2 and Bax. Leukemia 1999;13:266-74.
39. Buggins AG, Pepper C, Patten PE, Hewamana S, Gohil S, Moorhead J, et al. Interaction with vascular endothelium enhances survival in primary chronic lymphocytic leukemia cells via NF-kappaB activation and de novo gene transcription. Cancer Res 2010;70:7523-33.
40. Buchner M, Baer C, Prinz G, Dierks C, Burger M, Zenz T, et al. Spleen tyrosine kinase inhibition prevents chemokine-and integrin-mediated stromal protective effects in chronic lymphocytic leukemia. Blood 2010; 115:4497-506.
41. Herman SE, Mustafa RZ, Gyamfi JA, Pittaluga S, Chang S, Chang B, et al. Ibrutinib inhibits BCR and NF-kappaB signaling and reduces tumor proliferation in tissue-resident cells of patients with CLL. Blood 2014;123:3286-95.
42. Wodarz D, Garg N, Komarova NL, Benjamini O, Keating MJ, Wierda WG, et al. Kinetics of chronic lymphocytic leukemia (CLL) cells in tissues and blood during therapy with the BTK inhibitor ibrutinib. Blood 2014;123: 4132-5.
43. Andritsos L, Byrd JC, Jones JA, Hewes B, Kipps TJ, Hsu FJ, Burger JA. Preliminary results from a phase i dose escalation study to determine the maximum tolerated dose of plerixafor in combination with rituximab in patients with relapsed chronic lymphocytic leukemia. American Society of Hematology; 2010; Orlando, FL: Blood; 2010. p. Abstract 772.
44. Rettig MP, Ansstas G, DiPersio JF. Mobilization of hematopoietic stem and progenitor cells using inhibitors of CXCR4 and VLA-4. Leukemia 2012;26: 34-53.
45. Burger JA, Peled A. CXCR4 antagonists: targeting the microenvironment in leukemia and other cancers. Leukemia 2009;23:43-52.
46. Uy GL, Rettig MP, Motabi IH, McFarland K, Trinkaus KM, Hladnik LM, et al. A phase 1/2 study of chemosensitization with the CXCR4 antagonist plerixafor in relapsed or refractory acute myeloid leukemia. Blood 2012;119:3917-24.
47. O'Brien SM, Barrientos JC, Flinn IW, Barr PM, Burger JA, Navarro T, et al. Combination of the Bruton's tyrosine kinase (BTK) inhibitor PCI-32765 with bendamustine (B)/rituximab (R) (BR) in patients (pts) with relapsed/refractory (R/R) chronic lymphocytic leukemia (CLL): Interim results of a phase Ib/II study. ASCO Annual Meeting; 2012; Chicago, IL.
48. Barrientos JC, Barr PM, Flinn I, Burger JA, Salman Z, Clow F, et al. Ibrutinib in combination withbendamustine andrituximabisactiveand tolerable in patients with relapsed/refractory CLL/SLL: final results of a phase 1b study. Blood 2013;122:525.
49. Burger JA, Keating MJ, Wierda WG, Hartmann E, Hoellenriegel J, Rosin NY, et al. Safety and activity of ibrutinib plus rituximab for patients with high-risk chronic lymphocytic leukaemia: a single-arm, phase 2 study. Lancet Oncol 2014;15:1090-9.
50. Jaglowski SM, Jones JA, Flynn JM, Andritsos LA, Maddocks KJ, Woyach JA, et al. A phase 1b/2 study evaluating activity and tolerability of the BTK inhibitor ibrutinib in combination with ofatumumab in patients with chronic lymphocytic leukemia/small lymphocytic lymphoma (CLL/SLL) and related diseases. ASCO Annual Meeting 2014; Chicago, IL; 2014.