The Link of mRNA and rRNA Transcription by PUF60/FIR through TFIIH/P62 as a Novel Therapeutic Target for Cancer

Int J Mol Sci. 2023 Dec 11;24(24):17341. doi: 10.3390/ijms242417341.

Abstract

The interaction between mRNA and ribosomal RNA (rRNA) transcription in cancer remains unclear. RNAP I and II possess a common N-terminal tail (NTT), RNA polymerase subunit RPB6, which interacts with P62 of transcription factor (TF) IIH, and is a common target for the link between mRNA and rRNA transcription. The mRNAs and rRNAs affected by FUBP1-interacting repressor (FIR) were assessed via RNA sequencing and qRT-PCR analysis. An FIR, a c-myc transcriptional repressor, and its splicing form FIRΔexon2 were examined to interact with P62. Protein interaction was investigated via isothermal titration calorimetry measurements. FIR was found to contain a highly conserved region homologous to RPB6 that interacts with P62. FIRΔexon2 competed with FIR for P62 binding and coactivated transcription of mRNAs and rRNAs. Low-molecular-weight chemical compounds that bind to FIR and FIRΔexon2 were screened for cancer treatment. A low-molecular-weight chemical, BK697, which interacts with FIRΔexon2, inhibited tumor cell growth with rRNA suppression. In this study, a novel coactivation pathway for cancer-related mRNA and rRNA transcription through TFIIH/P62 by FIRΔexon2 was proposed. Direct evidence in X-ray crystallography is required in further studies to show the conformational difference between FIR and FIRΔexon2 that affects the P62-RBP6 interaction.

Keywords: FUBP1-interacting repressor (FIR); RPB6 of RNA polymerase (RNAP); aberrant RNA splicing; ribosomal RNA (rRNA); transcription factor IIH (TFIIH) P62 PH (pleckstrin homology).

MeSH terms

  • Alternative Splicing
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Humans
  • Neoplasms* / drug therapy
  • Neoplasms* / genetics
  • RNA Splicing Factors / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / metabolism
  • Repressor Proteins* / genetics
  • Transcription Factor TFIIH / genetics
  • Transcription Factor TFIIH / metabolism

Substances

  • RNA Splicing Factors
  • RNA, Messenger
  • Repressor Proteins
  • Transcription Factor TFIIH
  • FUBP1 protein, human
  • DNA-Binding Proteins
  • RNA-Binding Proteins

Grants and funding

This study was supported in part by Grant-in-Aid 26460667 for priority areas in cancer research from the Ministry of Education, Science, Sports and Culture of Japan (KAKENHI), 19kk0305007h9903 from AMED (Japan Agency for Medical Research and Development), the Chiba Foundation for Health Promotion and Disease Prevention, and was partly supported by Extramural Collaborative Research Grant of Cancer Research Institute, Kanazawa University to K.M.