Ibrutinib interferes with the cell-mediated anti-tumor activities of therapeutic CD20 antibodies: Implications for combination therapy

Haematologica

Volumn 100, Issue 1, 2015, Pages 77-86

  Da Roit, Fabio ^a   Engelberts, Patrick J ^b   Taylor, Ronald P ^c   Breij, Esther C W ^b   Gritti, Giuseppe ^a   Rambaldi, Alessandro ^a   Introna, Martino ^a   Parren, Paul W H I ^b,d   Beurskens, Frank J ^b   Golay, Josée ^a  

^a Azienda Ospedaliera Papa Giovanni XXIII   (Italy)

^b GENMAB   (Netherlands)

^c UNIVERSITY OF VIRGINIA   (United States)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIBODY; IBRUTINIB; IDELALISIB; OBINUTUZUMAB; OFATUMUMAB; RITUXIMAB; TRASTUZUMAB; ANTINEOPLASTIC AGENT; CD20 ANTIGEN; MONOCLONAL ANTIBODY; PURINE DERIVATIVE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; QUINAZOLINONE DERIVATIVE;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ACTIVATION; CELL GROWTH; CHRONIC LYMPHATIC LEUKEMIA; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DEGRANULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LARGE CELL LYMPHOMA; MACROPHAGE; NATURAL KILLER CELL; NEUTROPHIL; PHAGOCYTOSIS; APOPTOSIS; CASE CONTROL STUDY; CELL CULTURE; CELL PROLIFERATION; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOMA, B-CELL; PATHOLOGY; WESTERN BLOTTING;

ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD20; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CELL PROLIFERATION; CELLS, CULTURED; COMPLEMENT ACTIVATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; KILLER CELLS, NATURAL; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOMA, B-CELL; MACROPHAGES; NEUTROPHILS; PHAGOCYTOSIS; PURINES; PYRAZOLES; PYRIMIDINES; QUINAZOLINONES;

EID: 84920134814     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2014.107011     Document Type: Article

References (50)

1. Wierda WG, Kipps TJ, Mayer J, Stilgenbauer S, Williams CD, Hellmann A, et al. Ofatumumab as single-agent CD20 immunotherapy in fludarabine-refractory chronic lymphocytic leukemia. J Clin Oncol. 2010;28(10):1749-55.
2. Goede V, Fischer K, Busch R, Engelke A, Eichhorst B, Wendtner CM, et al. Obinutuzumab plus chlorambucil in Patients with CLL and coexisting Conditions. N Engl J Med. 2014;370(12): 1101-10.
3. Weiner GJ. Rituximab: mechanism of action. Semin Hematol. 2010;47(2):115-23.
4. Golay J, Da Roit F, Bologna L, Ferrara C, Leusen JH, Rambaldi A, et al. Glycoengineered CD20 antibody obinutuzumab activates neutrophils and mediates phagocytosis through CD16B more efficiently than rituximab. Blood 2013;122(20): 3482-91.
5. Teeling JL, Mackus WJ, Wiegman LJ, van den Brakel JH, Beers SA, French RR, et al. The biological activity of human CD20 monoclonal antibodies is linked to unique epitopes on CD20. J Immunol. 2006;177 (1):362-71.
6. Moessner E, Bruenker P, Moser S, Puentener U, Schmidt C, Herter S, et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 with enhanced direct and immune effector cell-mediated B-cell cytotoxicity. Blood. 2010;115(22):4393-402.
7. Bologna L, Gotti E, Manganini M, Rambaldi A, Intermesoli T, Introna M, et al. Mechanism of action of type II, glycoengineered, anti-CD20 monoclonal antibody GA101 in B-chronic lymphocytic leukemia whole blood assays in comparison with rituximab and alemtuzumab. J Immunol. 2011;186(6):3762-9.
8. Woyach JA, Johnson AJ, Byrd JC. The B-cell receptor signaling pathway as a therapeutic target in CLL. Blood 2012;120(6):1175-84.
9. 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(23):6287-96.
10. Burger JA, Chiorazzi N. B cell receptor signaling in chronic lymphocytic leukemia. Trends Immunol. 2013;34(12):592-601.
11. Buggy JJ, Elias L. Bruton tyrosine kinase (BTK) and its role in B-cell malignancy. Int Rev Immunol. 2012;31(2):119-32.
12. 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 (1):32-42.
13. Vargas L, Hamasy A, Nore BF, Smith CI. Inhibitors of BTK and ITK: state of the new drugs for cancer, autoimmunity and inflammatory diseases. Scand J Immunol. 2013;78 (2):130-9.
14. 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(1):88-94.
15. Wang ML, Rule S, Martin P, Goy A, Auer R, Kahl BS, et al. Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N Engl J Med. 2013;369(6):507-16.
16. Blum KA, Christian B, Flynn JM, Jaglowski SM, Jones JA, Maddocks K, et al. A phase I trial of the Bruton's tyrosine kinase (BTK) inhibitor, ibrutinib (PCI-32765), in combination with rituximab (R) and bendamustine in patients with relapsed/refractory non Hodgkin's lymphoma (NHL). Blood. 2012; 120(21):a1643.
17. Burger JA, Keating MJ, Wierda W, Hoellenriegel J, Jeyakumar G, Ferrajoli A, et al. Ibrutinib in combination with rituximab (iR) is well tolerated and induces high rate of durable remissions in patients with high-risk chronic lymphocytic leukemia (CLL): New, updated results of a phase II trial in 40 patients. Blood. 2013;122(21):a675.
18. Hallek M. Signaling the end of chronic lymphocytic leukemia: new frontline treatment strategies. Blood. 2013;122(23):3723-34.
19. Furman RR, Sharman JP, Coutre SE, Cheson BD, Pagel JM, Hillmen P, et al. Idelalisib and rituximab in relapsed chronic lymphocytic leukemia. N Engl J Med. 2014; 370(11):997-1007.
20. Gopal AK, Kahl BS, de Vos S, Wagner- Johnston ND, Schuster SJ, Jurczak WJ, et al. PI3Kdelta inhibition by idelalisib in patients with relapsed indolent lymphoma. N Engl J Med. 2014;370(11):1008-18.
21. Golay J, Lazzari M, Facchinetti V, Bernasconi S, Borleri G, Barbui T, et al. CD20 levels determine the in vitro susceptibility to rituximab and complement of Bcell chronic lymphocytic leukemia: further regulation by CD55 and CD59. Blood. 2001; 98(12):3383-9.
22. Bologna L, Gotti E, Da Roit F, Intermesoli T, Rambaldi A, Introna M, et al. Ofatumumab is more efficient than rituximab in lysing B chronic lymphocytic leukemia cells in whole blood and in combination with chemotherapy. J Immunol. 2013;190(1):231-9.
23. Mollnes TE, Brekke OL, Fung M, Fure H, Christiansen D, Bergseth G, et al. Essential role of the C5a receptor in E coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood. 2002;100(5):1869-77.
24. Lindorfer MA, Jinivizian HB, Foley PL, Kennedy AD, Solga MD, Taylor RP. B cell complement receptor 2 transfer reaction. J Immunol. 2003;170(7):3671-8.
25. Leidi M, Gotti E, Bologna L, Miranda E, Rimoldi M, Sica A, et al. M2 macrophages phagocytose rituximab-opsonized leukemic targets more efficiently than m1 cells in vitro. J Immunol. 2009;18(7)2:4415-22.
26. Herter S, Herting F, Mundigl O, Waldhauer I, Weinzierl T, Fauti T, et al. Preclinical activity of the type II CD20 antibody GA101 (obinutuzumab) compared with rituximab and ofatumumab in vitro and in xenograft models. Mol Cancer Ther. 2013;12(10):2031-42.
27. Ivanov A, Beers SA, Walshe CA, Honeychurch J, Alduaij W, Cox KL, et al. Monoclonal antibodies directed to CD20 and HLA-DR can elicit homotypic adhesion followed by lysosome-mediated cell death in human lymphoma and leukemia cells. J Clin Invest. 2009;119(8):2143-59.
28. Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti- CD20 monoclonal antibody and polymorphism in IgG Fc receptor Fc gammaIIIa gene. Blood. 2002;99(3):754-8.
29. Cheng S, Ma J, Guo A, Lu P, Leonard JP, Coleman M, et al. BTK inhibition targets in vivo CLL proliferation through its effects on B-cell receptor signaling activity. Leukemia. 2013;28(3):649-57.
30. Rahal R, Frick M, Romero R, Korn JM, Kridel R, Chun Chan F, et al. Pharmacological and genomic profiling identifies NF-kappaB-targeted treatment strategies for mantle cell lymphoma. Nat Med. 2014;20(1):87-92.
31. Yang Y, Shaffer AL, 3rd, Emre NC, Ceribelli M, Zhang M, Wright G, et al. Exploiting synthetic lethality for the therapy of ABC diffuse large B cell lymphoma. Cancer Cell. 2012;21(6):723-37.
32. Teeling JL, French RR, Cragg MS, van den Brakel J, Pluyter M, Huang H, et al. Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas. Blood. 2004;104(6):1793-800.
33. Beurskens FJ, Lindorfer MA, Farooqui M, Beum PV, Engelberts P, Mackus WJ, et al. Exhaustion of cytotoxic effector systems may limit monoclonal antibody-based immunotherapy in cancer patients. J Immunol. 2012;188(7):3532-41.
34. Bojarczuk K, Siernicka M, Dwojak M, Bobrowicz M, Pyrzynska B, Gaj P, et al. Bcell receptor pathway inhibitors affect CD20 levels and impair antitumor activity of anti- CD20 monoclonal antibodies. Leukemia. 2014;28(5):1163-7.
35. Chang BY, Francesco M, De Rooij MF, Magadala P, Steggerda SM, Huang MM, et al. Egress of CD19(+)CD5(+) cells into peripheral blood following treatment with the Bruton tyrosine kinase inhibitor ibrutinib in mantle cell lymphoma patients. Blood. 2013;122(14):2412-24.
36. Ponader S, Chen SS, Buggy JJ, Balakrishnan K, Gandhi V, Wierda WG, et al. The Bruton tyrosine kinase inhibitor PCI-32765 thwarts chronic lymphocytic leukemia cell survival and tissue homing in vitro and in vivo. Blood. 2012;119(5):1182-9.
37. Fiorcari S, Brown WS, McIntyre BW, Estrov Z, Maffei R, O'Brien S, et al. The PI3-kinase delta inhibitor idelalisib (GS-1101) targets integrin-mediated adhesion of chronic lymphocytic leukemia (CLL) cell to endothelial and marrow stromal cells. PLoS One 2013;8(12):e83830.
38. Kohrt HE, Sagiv-Barfi I, Rafiq S, Herman SE, Butchar JP, Cheney C, et al. Ibrutinib antagonizes rituximab-dependent NK cell-mediated cytotoxicity. Blood. 2014;123(12):1957-60.
39. Bao Y, Zheng J, Han C, Jin J, Han H, Liu Y, et al. Tyrosine kinase Btk is required for NK cell activation. J Biol Chem. 2012;287(28): 23769-78.
40. Dubovsky JA, Beckwith KA, Natarajan G, Woyach JA, Jaglowski S, Zhong Y, et al. Ibrutinib is an irreversible molecular inhibitor of ITK driving a Th1-selective pressure in T lymphocytes. Blood. 2013;122(15): 2539-49.
41. Berg LJ, Finkelstein LD, Lucas JA, Schwartzberg PL. Tec family kinases in T lymphocyte development and function. Annu Rev Immunol. 2005;23(1):549-600.
42. Khurana D, Arneson LN, Schoon RA, Dick CJ, Leibson PJ. Differential regulation of human NK cell-mediated cytotoxicity by the tyrosine kinase Itk. J Immunol. 2007; 178(6):3575-82.
43. Burger JA, Buggy JJ. Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765). Leuk Lymphoma. 2013;54(11):2385-91.
44. Lindvall JM, Blomberg KE, Valiaho J, Vargas L, Heinonen JE, Berglof A, et al. Bruton's tyrosine kinase: cell biology, sequence conservation, mutation spectrum, siRNA modifications, and expression profiling. Immunol Rev. 2005;203(1):200-15.
45. Jongstra-Bilen J, Puig Cano A, Hasija M, Xiao H, Smith CI, Cybulsky MI. Dual functions of Bruton's tyrosine kinase and Tec kinase during Fcgamma receptor-induced signaling and phagocytosis. J Immunol. 2008;181(1):288-98.
46. Ormsby T, Schlecker E, Ferdin J, Tessarz AS, Angelisova P, Koprulu AD, et al. Btk is a positive regulator in the TREM-1/DAP12 signaling pathway. Blood. 2011;118(4):936-45.
47. Uchida J, Hamaguchi Y, Oliver JA, Ravetch JV, Poe JC, Haas KM, et al. The innate mononuclear network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med. 2004;199(12): 1659-69.
48. Beers SA, Chan CH, James S, French RR, Attfield KE, Brennan CM, et al. Type II (tositumomab) anti-CD20 monoclonal antibody out performs type I (rituximab-like) reagents in B-cell depletion regardless of complement activation. Blood. 2008;112(10):4170-7.
49. Albanesi M, Mancardi DA, Macdonald LE, Iannascoli B, Zitvogel L, Murphy AJ, et al. Cutting edge: FcgammaRIII (CD16) and FcgammaRI (CD64) are responsible for anti-glycoprotein 75 monoclonal antibody TA99 therapy for experimental metastatic B16 melanoma. J Immunol. 2012;189(12): 5513-7.
50. Montalvao F, Garcia Z, Celli S, Breart B, Deguine J, Van Rooijen N, et al. The mechanism of anti-CD20-mediated B cell depletion revealed by intravital imaging. J Clin Invest. 2013;123(12):5098-103.