Development of RNA-FISH Assay for Detection of Oncogenic FGFR3-TACC3 Fusion Genes in FFPE Samples

PLoS One. 2016 Dec 8;11(12):e0165109. doi: 10.1371/journal.pone.0165109. eCollection 2016.

Abstract

Introduction and objectives: Oncogenic FGFR3-TACC3 fusions and FGFR3 mutations are target candidates for small molecule inhibitors in bladder cancer (BC). Because FGFR3 and TACC3 genes are located very closely on chromosome 4p16.3, detection of the fusion by DNA-FISH (fluorescent in situ hybridization) is not a feasible option. In this study, we developed a novel RNA-FISH assay using branched DNA probe to detect FGFR3-TACC3 fusions in formaldehyde-fixed paraffin-embedded (FFPE) human BC samples.

Materials and methods: The RNA-FISH assay was developed and validated using a mouse xenograft model with human BC cell lines. Next, we assessed the consistency of the RNA-FISH assay using 104 human BC samples. In this study, primary BC tissues were stored as frozen and FFPE tissues. FGFR3-TACC3 fusions were independently detected in FFPE sections by the RNA-FISH assay and in frozen tissues by RT-PCR. We also analyzed the presence of FGFR3 mutations by targeted sequencing of genomic DNA extracted from deparaffinized FFPE sections.

Results: FGFR3-TACC3 fusion transcripts were identified by RNA-FISH and RT-PCR in mouse xenograft FFPE tissues using the human BC cell lines RT112 and RT4. These cell lines have been reported to be fusion-positive. Signals for FGFR3-TACC3 fusions by RNA-FISH were positive in 2/60 (3%) of non-muscle-invasive BC (NMIBC) and 2/44 (5%) muscle-invasive BC (MIBC) patients. The results of RT-PCR of all 104 patients were identical to those of RNA-FISH. FGFR3 mutations were detected in 27/60 (45%) NMIBC and 8/44 (18%) MIBC patients. Except for one NMIBC patient, FGFR3 mutation and FGFR3-TACC3 fusion were mutually exclusive.

Conclusions: We developed an RNA-FISH assay for detection of the FGFR3-TACC3 fusion in FFPE samples of human BC tissues. Screening for not only FGFR3 mutations, but also for FGFR3-TACC3 fusion transcripts has the potential to identify additional patients that can be treated with FGFR inhibitors.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Cell Line, Tumor
  • DNA Probes / genetics
  • Female
  • Formaldehyde
  • Humans
  • In Situ Hybridization, Fluorescence / methods*
  • Male
  • Mice
  • Microtubule-Associated Proteins / genetics*
  • Middle Aged
  • Neoplasm Transplantation
  • Oncogene Fusion / genetics*
  • Paraffin Embedding
  • RNA / genetics*
  • Receptor, Fibroblast Growth Factor, Type 3 / genetics*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Urinary Bladder Neoplasms / genetics

Substances

  • DNA Probes
  • Microtubule-Associated Proteins
  • TACC3 protein, human
  • Formaldehyde
  • RNA
  • FGFR3 protein, human
  • Receptor, Fibroblast Growth Factor, Type 3

Grants and funding

The study was funded by Astellas (H.N.), and designed and analyzed by the authors in collaboration with Astellas. Astellas had a role in the design and conduct of the study; management, analysis, and interpretation of the data; and preparation, review, and approval of the manuscript. This work was also supported in part by a Grant-in-Aid for Challenging Exploratory Research (H.N.) (grant number 26670696) and a Grant-in-Aid for Scientific Research B (H.N.) (grant number 26293349) from the Japan Society for the Promotion of Science (JSPS) (https://www.jsps.go.jp/english/). The JSPS had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.