Constitutive β-Catenin Overexpression Represses Lncrna MIR100HG Transcription via HDAC6-Mediated Histone Modification in Colorectal Cancer

Mol Cancer Res. 2022 Jun 3;20(6):949-959. doi: 10.1158/1541-7786.MCR-21-0923.

Abstract

Wnt/β-catenin signaling plays a critical role in colonic carcinogenesis. However, non-coding RNAs (ncRNA) transcriptionally regulated by β-catenin are largely unknown. Herein, we found that lncRNA MIR100HG (lnc-MIR100HG) negatively correlated with target genes of β-catenin from The Cancer Genome Atlas colorectal carcinoma database, which was verified in 48 paired colorectal carcinoma specimens. In addition, constitutive overexpression of β-catenin decreased primary and mature lnc-MIR100HG levels, whereas blockage of β-catenin activity with siRNA or inhibitors significantly increased their expression. DNA pull-down and chromatin immunoprecipitation revealed the binding of β-catenin/TCF4 to the MIR100HG promoter. Moreover, β-catenin-forced expression reduced the enrichment of H3K27Ac, an active transcription marker, on the promoter, whereas β-catenin inhibition reversed this effect. Furthermore, HDAC6 was recruited to the MIR100HG promoter and downregulated H3K27Ac enrichment in a β-catenin-dependent manner. Besides, HDAC6 was upregulated and negatively correlated with lnc-MIR100HG in colorectal carcinoma specimens. Functional studies showed that lnc-MIR100HG overexpression induced cell-cycle G0-G1 arrest and repressed cell proliferation via p57 upregulation in vitro and in vivo. Taken together, we found that ectopic β-catenin transcriptionally repressed lnc-MIR100HG expression through HDAC6-mediated histone modification in colorectal carcinoma. Lnc-MIR100HG regulates the cell cycle through p57.

Implications: It provides a novel downstream mechanism highlighting β-catenin action during colon carcinogenesis and may shed light for further therapeutic approaches.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carcinogenesis / genetics
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Colorectal Neoplasms* / pathology
  • Gene Expression Regulation, Neoplastic
  • Histone Code
  • Histone Deacetylase 6 / metabolism
  • Humans
  • RNA, Long Noncoding* / genetics
  • Wnt Signaling Pathway / genetics
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • CTNNB1 protein, human
  • RNA, Long Noncoding
  • beta Catenin
  • HDAC6 protein, human
  • Histone Deacetylase 6