Methyltransferase Inhibition Enables Tgf β Driven Induction of CDKN2A and B in Cancer Cells

Mol Cell Biol. 2023;43(3):115-129. doi: 10.1080/10985549.2023.2186074.

Abstract

CDKN2A/B deletion or silencing is common across human cancer, reinforcing the general importance of bypassing its tumor suppression in cancer formation or progression. In rhabdomyosarcoma (RMS) and neuroblastoma, two common childhood cancers, the three CDKN2A/B transcripts are independently expressed to varying degrees, but one, ARF, is uniformly silenced. Although TGFβ induces certain CDKN2A/B transcripts in HeLa cells, it was unable to do so in five tested RMS lines unless the cells were pretreated with a broadly acting methyltransferase inhibitor, DZNep, or one targeting EZH2. CDKN2A/B induction by TGFβ correlated with de novo appearance of three H3K27Ac peaks within a 20 kb cis element ∼150 kb proximal to CDKN2A/B. Deleting that segment prevented their induction by TGFβ but not a basal increase driven by methyltransferase inhibition alone. Expression of two CDKN2A/B transcripts was enhanced by dCas9/CRISPR activation targeting either the relevant promoter or the 20 kb cis elements, and this "precise" manipulation diminished RMS cell propagation in vitro. Our findings show crosstalk between methyltransferase inhibition and TGFβ-dependent activation of a remote enhancer to reverse CDKN2A/B silencing. Though focused on CDKN2A/B here, such crosstalk may apply to other TGFβ-responsive genes and perhaps govern this signaling protein's complex effects promoting or blocking cancer.

Keywords: CDKN2A/B; Cis enhancers; EZH2; chromosome 9p21; histone methyltransferase.

Publication types

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

MeSH terms

  • Cell Line, Tumor
  • Cyclin-Dependent Kinase Inhibitor p15* / genetics
  • Cyclin-Dependent Kinase Inhibitor p15* / metabolism
  • Cyclin-Dependent Kinase Inhibitor p16* / genetics
  • Cyclin-Dependent Kinase Inhibitor p16* / metabolism
  • HeLa Cells
  • Humans
  • Methyltransferases* / antagonists & inhibitors
  • Neoplasms*
  • Transforming Growth Factor beta* / metabolism

Substances

  • CDKN2A protein, human
  • Cyclin-Dependent Kinase Inhibitor p16
  • Methyltransferases
  • Transforming Growth Factor beta
  • TGFB1 protein, human
  • CDKN2B protein, human
  • Cyclin-Dependent Kinase Inhibitor p15