RNAi screening of subtracted transcriptomes reveals tumor suppression by taurine-activated GABAA receptors involved in volume regulation

PLoS One. 2018 May 22;13(5):e0196979. doi: 10.1371/journal.pone.0196979. eCollection 2018.

Abstract

To identify coding and non-coding suppressor genes of anchorage-independent proliferation by efficient loss-of-function screening, we have developed a method for enzymatic production of low complexity shRNA libraries from subtracted transcriptomes. We produced and screened two LEGO (Low-complexity by Enrichment for Genes shut Off) shRNA libraries that were enriched for shRNA vectors targeting coding and non-coding polyadenylated transcripts that were reduced in transformed Mouse Embryonic Fibroblasts (MEFs). The LEGO shRNA libraries included ~25 shRNA vectors per transcript which limited off-target artifacts. Our method identified 79 coding and non-coding suppressor transcripts. We found that taurine-responsive GABAA receptor subunits, including GABRA5 and GABRB3, were induced during the arrest of non-transformed anchor-deprived MEFs and prevented anchorless proliferation. We show that taurine activates chloride currents through GABAA receptors on MEFs, causing seclusion of cell volume in large membrane protrusions. Volume seclusion from cells by taurine correlated with reduced proliferation and, conversely, suppression of this pathway allowed anchorage-independent proliferation. In human cholangiocarcinomas, we found that several proteins involved in taurine signaling via GABAA receptors were repressed. Low GABRA5 expression typified hyperproliferative tumors, and loss of taurine signaling correlated with reduced patient survival, suggesting this tumor suppressive mechanism operates in vivo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bile Duct Neoplasms / drug therapy
  • Bile Duct Neoplasms / genetics
  • Bile Duct Neoplasms / metabolism
  • Bile Duct Neoplasms / pathology
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Cholangiocarcinoma / drug therapy
  • Cholangiocarcinoma / genetics
  • Cholangiocarcinoma / metabolism
  • Cholangiocarcinoma / pathology*
  • Embryo, Mammalian / drug effects
  • Embryo, Mammalian / metabolism
  • Embryo, Mammalian / pathology*
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Neoplastic / drug effects
  • Genes, Tumor Suppressor
  • Humans
  • Mice
  • Prognosis
  • RNA Interference
  • RNA, Small Interfering / genetics
  • Receptors, GABA-A / genetics
  • Receptors, GABA-A / metabolism*
  • Signal Transduction / drug effects
  • Subtractive Hybridization Techniques
  • Survival Rate
  • Taurine / pharmacology*
  • Transcriptome / drug effects*

Substances

  • RNA, Small Interfering
  • Receptors, GABA-A
  • Taurine

Grants and funding

This work was supported by Netherlands Genomics Initiative Horizon Breakthrough Project 050-71-038 (CW, HTR), URL: www.zonmw.nl; Dutch Cancer Society NKI 2002-2634 (HTR), URL: www.kwf.nl; Netherlands Organization for Scientific Research ALW 819.02.013 (CW, HTR), URL: www.nwo.nl. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.