Detection, Characterization, and Inhibition of FGFR-TACC Fusions in IDH Wild-type Glioma

Clin Cancer Res. 2015 Jul 15;21(14):3307-17. doi: 10.1158/1078-0432.CCR-14-2199. Epub 2015 Jan 21.

Abstract

Purpose: Oncogenic fusions consisting of fibroblast growth factor receptor (FGFR) and TACC are present in a subgroup of glioblastoma (GBM) and other human cancers and have been proposed as new therapeutic targets. We analyzed frequency and molecular features of FGFR-TACC fusions and explored the therapeutic efficacy of inhibiting FGFR kinase in GBM and grade II and III glioma.

Experimental design: Overall, 795 gliomas (584 GBM, 85 grades II and III with wild-type and 126 with IDH1/2 mutation) were screened for FGFR-TACC breakpoints and associated molecular profile. We also analyzed expression of the FGFR3 and TACC3 components of the fusions. The effects of the specific FGFR inhibitor JNJ-42756493 for FGFR3-TACC3-positive glioma were determined in preclinical experiments. Two patients with advanced FGFR3-TACC3-positive GBM received JNJ-42756493 and were assessed for therapeutic response.

Results: Three of 85 IDH1/2 wild-type (3.5%) but none of 126 IDH1/2-mutant grade II and III gliomas harbored FGFR3-TACC3 fusions. FGFR-TACC rearrangements were present in 17 of 584 GBM (2.9%). FGFR3-TACC3 fusions were associated with strong and homogeneous FGFR3 immunostaining. They are mutually exclusive with IDH1/2 mutations and EGFR amplification, whereas they co-occur with CDK4 amplification. JNJ-42756493 inhibited growth of glioma cells harboring FGFR3-TACC3 in vitro and in vivo. The two patients with FGFR3-TACC3 rearrangements who received JNJ-42756493 manifested clinical improvement with stable disease and minor response, respectively.

Conclusions: RT-PCR sequencing is a sensitive and specific method to identify FGFR-TACC-positive patients. FGFR3-TACC3 fusions are associated with uniform intratumor expression of the fusion protein. The clinical response observed in the FGFR3-TACC3-positive patients treated with an FGFR inhibitor supports clinical studies of FGFR inhibition in FGFR-TACC-positive patients.

Publication types

  • Clinical Trial
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / therapeutic use*
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / genetics*
  • Brain Neoplasms / mortality
  • DNA Mutational Analysis / methods
  • Female
  • Fluorescent Antibody Technique
  • Glioma / drug therapy
  • Glioma / genetics*
  • Glioma / mortality
  • Humans
  • Immunohistochemistry
  • Isocitrate Dehydrogenase / genetics
  • Kaplan-Meier Estimate
  • Male
  • Mice
  • Mice, Nude
  • Microtubule-Associated Proteins / genetics
  • Molecular Targeted Therapy
  • Oncogene Proteins, Fusion / genetics*
  • Pyrazoles / therapeutic use*
  • Quinoxalines / therapeutic use*
  • Receptor, Fibroblast Growth Factor, Type 3 / genetics
  • Reverse Transcriptase Polymerase Chain Reaction / methods
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Microtubule-Associated Proteins
  • Oncogene Proteins, Fusion
  • Pyrazoles
  • Quinoxalines
  • TACC3 protein, human
  • erdafitinib
  • IDH2 protein, human
  • Isocitrate Dehydrogenase
  • IDH1 protein, human
  • FGFR3 protein, human
  • Receptor, Fibroblast Growth Factor, Type 3