Anti-tumor efficacy study of the Bruton’s tyrosine kinase (BTK) inhibitor, ONO/GS-4059, in combination with the glycoengineered type II anti-CD20 monoclonal antibody obinutuzumab (GA101) demonstrates superior in vivo efficacy compared to ONO/GS-4059 in combination with rituximab

References

• Qiu Y, Kung HJ. Signaling network of the BTK family kinases. Oncogene. 2000;19:5651–5661.
   PubMed Web of Science ®Google Scholar
• Tomlinson MG, Kane LP, Su J, et al. Expression and function of Tec, ITK, and BTK in lymphocytes: evidence for a unique role for Tec. Mol Cell Biol. 2004;24:2455–2466.
   PubMed Web of Science ®Google Scholar
• Musilova K, Mraz M. MicroRNAs in B-cell lymphomas: how a complex biology gets more complex. Leukemia. 2015;29:1004–1017.
   PubMed Web of Science ®Google Scholar
• de Gorter DJ, Beuling EA, Kersseboom R, et al. Bruton's tyrosine kinase and phospholipase Cgamma2 mediate chemokine-controlled B cell migration and homing. Immunity. 2007;26:93–104.
   PubMed Web of Science ®Google Scholar
• Moreau T, Calmels B, Barlogis V, et al. Potential application of gene therapy to X-linked agammaglobulinemia. Curr Gene Ther. 2007;7:284–294.
   PubMed Web of Science ®Google Scholar
• Hendriks RW, Yuvaraj S, Kil LP. Targeting Bruton's tyrosine kinase in B cell malignancies. Nat Rev Cancer. 2014;14:219–232.
   PubMed Web of Science ®Google Scholar
• Di Paolo JA, Huang T, Balazs M, et al. Specific BTK inhibition suppresses B cell- and myeloid cell-mediated arthritis. Nat Chem Biol. 2011;7:41–50.
   PubMed Web of Science ®Google Scholar
• Pan Z, Scheerens H, Li SJ, et al. Discovery of selective irreversible inhibitors for Bruton's tyrosine kinase. ChemMedChem. 2007;2:58–61.
   PubMed Web of Science ®Google Scholar
• Liu Q, Sabnis Y, Zhao Z, et al. Developing irreversible inhibitors of the protein kinase cysteinome. Chem Biol. 2013;20:146–159.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Furman RR, Coutre SE, et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N Engl J Med. 2013;369:32–42.
   PubMed Web of Science ®Google Scholar
• Wang ML, Rule S, Martin P, et al. Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N Engl J Med. 2013;369:507–516.
   PubMed Web of Science ®Google Scholar
• Treon SP, Tripsas CK, Meid K, et al. Ibrutinib in previously treated Waldenström's macroglobulinemia. N Engl J Med. 2015;372:1430–1440.
   PubMed Web of Science ®Google Scholar
• Honigberg LA, Smith AM, Sirisawad M, et al. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci USA. 2010;107:13075–13080.
   PubMed Web of Science ®Google Scholar
• Kohrt HE, Sagiv-Barfi I, Rafiq S, et al. Ibrutinib antagonizes rituximab-dependent NK cell-mediated cytotoxicity. Blood. 2014;123:1957–1960.
   PubMed Web of Science ®Google Scholar
• Rajasekaran N, Sadaram M, Hebb J, et al. Three BTK-specific inhibitors, in contrast to Ibrutinib, do not antagonize rituximab-dependent NK-cell mediated cytotoxicity. Blood. 2014;124:3118.
   PubMed Web of Science ®Google Scholar
• Khurana D, Arneson LN, Schoon RA, et al. Differential regulation of human NK cell-mediated cytotoxicity by the tyrosine kinase ITK. J Immunol. 2007;178:3575–3582.
   PubMed Web of Science ®Google Scholar
• Yoshizawa T, Ariza Y, Ueda Y, et al. Development of a Bruton's tyrosine kinase (BTK) inhibitor, ONO-4059: efficacy in a collagen induced arthritis (CIA) model indicates potential treatment for rheumatoid arthritis (RA). Arthritis Rheum. 2012;64:10.
   Google Scholar
• Kozaki R, Hutchinson C, Sandrine J, et al. Kinome reprogramming in DLBCL by the BTK-specific inhibitor ONO-4059 highlights synergistic combinations for clinical application. Haematologica. 2014;99:137–138.
   Web of Science ®Google Scholar
• Walter HS, Rule SA, Dyer MJ, et al. A phase 1 clinical trial of the selective BTK inhibitor ONO/GS-4059 in relapsed and refractory mature B-cell malignancies. Blood. 2016;127:411–419.
   PubMed Web of Science ®Google Scholar
• Wilson WH, Young RM, Schmitz R, et al. Targeting B cell receptor signaling with ibrutinib in diffuse large B cell lymphoma. Nat Med. 2015;21:922–926.
   PubMed Web of Science ®Google Scholar
• Mathews Griner LA, Guha R, Shinn P, et al. High-throughput combinatorial screening identifies drugs that cooperate with ibrutinib to kill activated B-cell-like diffuse large B-cell lymphoma cells. Proc Natl Acad Sci USA. 2014;111:2349–2354.
   PubMed Web of Science ®Google Scholar
• Herting F, Friess T, Bader S, et al. Enhanced anti-tumor activity of the glycoengineered type II CD20 antibody obinutuzumab (GA101) in combination with chemotherapy in xenograft models of human lymphoma. Leuk Lymphoma. 2014;55:2151–2160.
   PubMed Web of Science ®Google Scholar
• Tohda S, Sato T, Kogoshi H, et al. Establishment of a novel B-cell lymphoma cell line with suppressed growth by gamma-secretase inhibitors. Leuk Res. 2006;30:1385–1390.
   PubMed Web of Science ®Google Scholar
• Broussas M, Broyer L, Goetsch L. Evaluation of antibody-dependent cell cytotoxicity using lactate dehydrogenase (LDH) measurement. Methods Mol Biol. 2013;988:305–317.
   PubMedGoogle Scholar
• Epstein AL, Levy R, Kim H, et al. Biology of the human malignant lymphomas IV. Functional characterization of ten diffuse histiocytic lymphoma cell lines. Cancer. 1978;42:2379–2391.
   PubMed Web of Science ®Google Scholar
• Taji H, Kagami Y, Okada Y, et al. Growth inhibition of CD20-positive B lymphoma cell lines by IDEC-C2B8 anti-CD20 monoclonal antibody. Jpn J Cancer Res. 1998;89:748–756.
   PubMedGoogle Scholar
• Whang JA, Chang BY. Bruton's tyrosine kinase inhibitors for the treatment of rheumatoid arthritis. Drug Discov Today. 2014;19:1200–1204.
   PubMed Web of Science ®Google Scholar
• Davis C, Stepanchick E, Syed K, et al. Effects of ibrutinib on rituximab and GA101 induced antibody-dependent cell cytotoxicity (ADCC) in lymphoma cells in vitro. Blood. 2014;124:3117.
   Web of Science ®Google Scholar
• Kerbel RS. Human tumor xenografts as predictive preclinical models for anticancer drug activity in humans: better than commonly perceived-but they can be improved. Cancer Biol Ther. 2003;2:S134–S139.
   PubMed Web of Science ®Google Scholar
• Abrams TJ, Murray LJ, Pesenti E, et al. Preclinical evaluation of the tyrosine kinase inhibitor SU11248 as a single agent and in combination with “standard of care” therapeutic agents for the treatment of breast cancer. Mol Cancer Ther. 2003;10:1011–1021.
   Google Scholar
• Küppers R. Mechanisms of B-cell lymphoma pathogenesis. Nat Rev Cancer. 2005;5:251–262.
   PubMed Web of Science ®Google Scholar
• Lenz G, Wright G, Dave SS, et al. Stromal gene signatures in large-B-cell lymphomas. N Engl J Med. 2008;359:2313–2323.
   PubMed Web of Science ®Google Scholar
• Smith MR. Rituximab (monoclonal anti-CD20 antibody): mechanisms of action and resistance. Oncogene. 2003;22:7359–7368.
   PubMed Web of Science ®Google Scholar