Targeting Super-Enhancer-Associated Oncogenes in Osteosarcoma with THZ2, a Covalent CDK7 Inhibitor

Clin Cancer Res. 2020 Jun 1;26(11):2681-2692. doi: 10.1158/1078-0432.CCR-19-1418. Epub 2020 Jan 14.

Abstract

Purpose: Malignancy of cancer cells depends on the active transcription of tumor-associated genes. Recently, unique clusters of transcriptional enhancers, termed super-enhancers, have been reported to drive the expression of genes that define cell identity. In this study, we characterized specific super-enhancer-associated genes of osteosarcoma, and explored their potential therapeutic value.

Experimental design: Super-enhancer regions were characterized through chromatin immunoprecipitation sequencing (ChIP-seq). RT-qPCR was used to detect the mRNA level of CDK7 in patient specimens and confirm the regulation of sensitive oncogenes by THZ2. The phosphorylation of the initiation-associated sites of RNA polymerase II (RNAPII) C-terminal repeat domain (CTD) was measured using Western blotting. Microarray expression analysis was conducted to explore transcriptional changes after THZ2 treatment. A variety of in vitro and in vivo assays were performed to assess the effects of CDK7 knockdown and THZ2 treatment in osteosarcoma.

Results: Super-enhancers were associated with oncogenic transcripts and key genes encoding cell-type-specific transcription factors in osteosarcoma. Knockdown of transcription factor CDK7 reduced phosphorylation of the RNAPII CTD, and suppressed the growth and metastasis of osteosarcoma. A new specific CDK7 inhibitor, THZ2, suppressed cancer biology by inhibition of transcriptional activity. Compared with typical enhancers, osteosarcoma super-enhancer-associated oncogenes were particular vulnerable to this transcriptional disruption. THZ2 exhibited a powerful anti-osteosarcoma effect in vitro and in vivo.

Conclusions: Super-enhancer-associated genes contribute to the malignant potential of osteosarcoma, and selectively targeting super-enhancer-associated oncogenes with the specific CDK7 inhibitor THZ2 might be a promising therapeutic strategy for patients with osteosarcoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Bone Neoplasms / drug therapy*
  • Bone Neoplasms / enzymology
  • Bone Neoplasms / genetics
  • Bone Neoplasms / pathology
  • Cell Movement
  • Cell Proliferation
  • Cyclin-Dependent Kinase-Activating Kinase
  • Cyclin-Dependent Kinases / antagonists & inhibitors*
  • Cyclin-Dependent Kinases / genetics
  • Enhancer Elements, Genetic*
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Mice
  • Mice, Nude
  • Oncogenes
  • Osteosarcoma / drug therapy*
  • Osteosarcoma / enzymology
  • Osteosarcoma / genetics
  • Osteosarcoma / pathology
  • Phenylenediamines / chemistry
  • Prognosis
  • Protein Kinase Inhibitors / pharmacology*
  • Survival Rate
  • Tumor Cells, Cultured
  • Xenograft Model Antitumor Assays

Substances

  • Phenylenediamines
  • Protein Kinase Inhibitors
  • Cyclin-Dependent Kinases
  • Cyclin-Dependent Kinase-Activating Kinase