PI3Kδ inhibitor idelalisib in combination with BTK inhibitor ONO/GS-4059 in diffuse large B cell lymphoma with acquired resistance to PI3Kδ and BTK inhibitors

PLoS One. 2017 Feb 8;12(2):e0171221. doi: 10.1371/journal.pone.0171221. eCollection 2017.

Abstract

Activated B-cell-like diffuse large B-cell lymphoma relies on B-cell receptor signaling to drive proliferation and survival. Downstream of the B-cell receptor, the key signaling kinases Bruton's tyrosine kinase and phosphoinositide 3-kinase δ offer opportunities for therapeutic intervention by agents such as ibrutinib, ONO/GS-4059, and idelalisib. Combination therapy with such targeted agents could provide enhanced efficacy due to complimentary mechanisms of action. In this study, we describe both the additive interaction of and resistance mechanisms to idelalisib and ONO/GS-4059 in a model of activated B-cell-like diffuse large B-cell lymphoma. Significant tumor regression was observed with a combination of PI3Kδ and Bruton's tyrosine kinase inhibitors in the mouse TMD8 xenograft. Acquired resistance to idelalisib in the TMD8 cell line occurred by loss of phosphatase and tensin homolog and phosphoinositide 3-kinase pathway upregulation, but not by mutation of PIK3CD. Sensitivity to idelalisib could be restored by combining idelalisib and ONO/GS-4059. Further evaluation of targeted inhibitors revealed that the combination of idelalisib and the phosphoinositide-dependent kinase-1 inhibitor GSK2334470 or the AKT inhibitor MK-2206 could partially overcome resistance. Characterization of acquired Bruton's tyrosine kinase inhibitor resistance revealed a novel tumor necrosis factor alpha induced protein 3 mutation (TNFAIP3 Q143*), which led to a loss of A20 protein, and increased p-IκBα. The combination of idelalisib and ONO/GS-4059 partially restored sensitivity in this resistant line. Additionally, a mutation in Bruton's tyrosine kinase at C481F was identified as a mechanism of resistance. The combination activity observed with idelalisib and ONO/GS-4059, taken together with the ability to overcome resistance, could lead to a new therapeutic option in activated B-cell-like diffuse large B-cell lymphoma. A clinical trial is currently underway to evaluate the combination of idelalisib and ONO/GS-4059 (NCT02457598).

MeSH terms

  • 3-Phosphoinositide-Dependent Protein Kinases / metabolism
  • Agammaglobulinaemia Tyrosine Kinase
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Drug Resistance, Neoplasm*
  • Humans
  • Imidazoles / pharmacology*
  • Lymphoma, Large B-Cell, Diffuse / drug therapy
  • Lymphoma, Large B-Cell, Diffuse / metabolism*
  • Mutation
  • PTEN Phosphohydrolase / metabolism
  • Phosphoinositide-3 Kinase Inhibitors*
  • Protein-Tyrosine Kinases / antagonists & inhibitors*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Purines / pharmacology*
  • Pyrimidines / pharmacology*
  • Quinazolinones / pharmacology*
  • Signal Transduction / drug effects

Substances

  • Antineoplastic Agents
  • Imidazoles
  • Phosphoinositide-3 Kinase Inhibitors
  • Purines
  • Pyrimidines
  • Quinazolinones
  • Protein-Tyrosine Kinases
  • Agammaglobulinaemia Tyrosine Kinase
  • BTK protein, human
  • Btk protein, mouse
  • 3-Phosphoinositide-Dependent Protein Kinases
  • PDPK1 protein, human
  • Proto-Oncogene Proteins c-akt
  • PTEN Phosphohydrolase
  • tirabrutinib
  • idelalisib

Associated data

  • ClinicalTrials.gov/NCT02457598

Grants and funding

This study was funded by Gilead Sciences, Inc. Since all authors were employees of the study sponsor at the time the study was conducted, the sponsor was involved in the study design, data collection and analysis, decision to publish, and preparation of the manuscript.