Regulation of RNA polymerase III transcription during transformation of human IMR90 fibroblasts with defined genetic elements

Cell Cycle. 2018;17(5):605-615. doi: 10.1080/15384101.2017.1405881. Epub 2018 Jan 22.

Abstract

RNA polymerase (Pol) III transcribes small untranslated RNAs that are essential for cellular homeostasis and growth. Its activity is regulated by inactivation of tumor suppressor proteins and overexpression of the oncogene c-MYC, but the concerted action of these tumor-promoting factors on Pol III transcription has not yet been assessed. In order to comprehensively analyse the regulation of Pol III transcription during tumorigenesis we employ a model system that relies on the expression of five genetic elements to achieve cellular transformation. Expression of these elements in six distinct transformation intermediate cell lines leads to the inactivation of TP53, RB1, and protein phosphatase 2A, as well as the activation of RAS and the protection of telomeres by TERT, thereby conducting to full tumoral transformation of IMR90 fibroblasts. Transformation is accompanied by moderately enhanced levels of a subset of Pol III-transcribed RNAs (7SK; MRP; H1). In addition, mRNA and/or protein levels of several Pol III subunits and transcription factors are upregulated, including increased protein levels of TFIIIB and TFIIIC subunits, of SNAPC1 and of Pol III subunits. Strikingly, the expression of POLR3G and of SNAPC1 is strongly enhanced during transformation in this cellular transformation model. Collectively, our data indicate that increased expression of several components of the Pol III transcription system accompanied by a 2-fold increase in steady state levels of a subset of Pol III RNAs is sufficient for sustaining tumor formation.

Keywords: 7SK RNA; POLR3G; PP2A; RAS; RB1; RNA polymerase III; TERT; TP53; defined transformation; transcription.

Publication types

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

MeSH terms

  • Animals
  • Cell Transformation, Neoplastic
  • Female
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Humans
  • Mice
  • Mice, Nude
  • Mice, SCID
  • Models, Biological
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • RNA Polymerase III / genetics
  • RNA Polymerase III / metabolism*
  • Retinoblastoma Binding Proteins / genetics
  • Retinoblastoma Binding Proteins / metabolism
  • Telomerase / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription, Genetic*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Up-Regulation

Substances

  • Protein Subunits
  • Retinoblastoma Binding Proteins
  • SNAPC1 protein, human
  • Transcription Factors
  • Tumor Suppressor Protein p53
  • POLR3G protein, human
  • Telomerase
  • RNA Polymerase III