Pervasive transcription read-through promotes aberrant expression of oncogenes and RNA chimeras in renal carcinoma

Elife. 2015 Nov 17:4:e09214. doi: 10.7554/eLife.09214.

Abstract

Aberrant expression of cancer genes and non-canonical RNA species is a hallmark of cancer. However, the mechanisms driving such atypical gene expression programs are incompletely understood. Here, our transcriptional profiling of a cohort of 50 primary clear cell renal cell carcinoma (ccRCC) samples from The Cancer Genome Atlas (TCGA) reveals that transcription read-through beyond the termination site is a source of transcriptome diversity in cancer cells. Amongst the genes most frequently mutated in ccRCC, we identified SETD2 inactivation as a potent enhancer of transcription read-through. We further show that invasion of neighbouring genes and generation of RNA chimeras are functional outcomes of transcription read-through. We identified the BCL2 oncogene as one of such invaded genes and detected a novel chimera, the CTSC-RAB38, in 20% of ccRCC samples. Collectively, our data highlight a novel link between transcription read-through and aberrant expression of oncogenes and chimeric transcripts that is prevalent in cancer.

Keywords: BCL2 oncogene; RNA chimeras; cancer genes; chromosomes; clear cell renal cell carcinoma; genes; human; human biology; medicine; transcription read-through.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carcinoma, Renal Cell / pathology*
  • Cell Line, Tumor
  • Gene Expression Profiling
  • Gene Expression*
  • Histone-Lysine N-Methyltransferase / metabolism
  • Humans
  • Kidney Neoplasms / pathology*
  • Oncogene Proteins / biosynthesis*
  • Oncogene Proteins / genetics
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • RNA, Messenger / biosynthesis*
  • RNA, Messenger / genetics
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / genetics
  • Recombination, Genetic*
  • Transcription, Genetic*

Substances

  • BCL2 protein, human
  • Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • RNA, Messenger
  • Recombinant Fusion Proteins
  • Histone-Lysine N-Methyltransferase
  • SETD2 protein, human

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.