First-in-Class Inhibitors of Oncogenic CHD1L with Preclinical Activity against Colorectal Cancer

Mol Cancer Ther. 2020 Aug;19(8):1598-1612. doi: 10.1158/1535-7163.MCT-20-0106. Epub 2020 Jun 4.

Abstract

Since the discovery of CHD1L in 2008, it has emerged as an oncogene implicated in the pathology and poor prognosis of a variety of cancers, including gastrointestinal cancers. However, a mechanistic understanding of CHD1L as a driver of colorectal cancer has been limited. Until now, there have been no reported inhibitors of CHD1L, also limiting its development as a molecular target. We sought to characterize the clinicopathologic link between CHD1L and colorectal cancer, determine the mechanism(s) by which CHD1L drives malignant colorectal cancer, and discover the first inhibitors with potential for novel treatments for colorectal cancer. The clinicopathologic characteristics associated with CHD1L expression were evaluated using microarray data from 585 patients with colorectal cancer. Further analysis of microarray data indicated that CHD1L may function through the Wnt/TCF pathway. Thus, we conducted knockdown and overexpression studies with CHD1L to determine its role in Wnt/TCF-driven epithelial-to-mesenchymal transition (EMT). We performed high-throughput screening (HTS) to identify the first CHD1L inhibitors. The mechanism of action, antitumor efficacy, and drug-like properties of lead CHD1L inhibitors were determined using biochemical assays, cell models, tumor organoids, patient-derived tumor organoids, and in vivo pharmacokinetics and pharmacodynamics. Lead CHD1L inhibitors display potent in vitro antitumor activity by reversing TCF-driven EMT. The best lead CHD1L inhibitor possesses drug-like properties in pharmacokinetic/pharmacodynamic mouse models. This work validates CHD1L as a druggable target and establishes a novel therapeutic strategy for the treatment of colorectal cancer.

Publication types

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

MeSH terms

  • Adenocarcinoma / drug therapy*
  • Adenocarcinoma / mortality
  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use*
  • Antineoplastic Agents / toxicity
  • Apoptosis
  • Cell Line, Tumor
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / mortality
  • DNA Damage
  • DNA Helicases / antagonists & inhibitors*
  • DNA Helicases / genetics
  • DNA Helicases / physiology
  • DNA-Binding Proteins / antagonists & inhibitors*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology
  • Drug Screening Assays, Antitumor
  • Enzyme Inhibitors / pharmacology
  • Enzyme Inhibitors / therapeutic use*
  • Enzyme Inhibitors / toxicity
  • Epithelial-Mesenchymal Transition / drug effects
  • Epithelial-Mesenchymal Transition / physiology
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Gene Knockdown Techniques
  • High-Throughput Screening Assays
  • Humans
  • Kaplan-Meier Estimate
  • Mice
  • Neoplasm Proteins / antagonists & inhibitors*
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology
  • Organoids / drug effects
  • RNA, Messenger / biosynthesis
  • RNA, Neoplasm / biosynthesis
  • Recombinant Proteins / metabolism
  • Small Molecule Libraries
  • TCF Transcription Factors / physiology
  • Transcription, Genetic / drug effects
  • Wnt Signaling Pathway / drug effects
  • Wnt Signaling Pathway / genetics
  • Wnt Signaling Pathway / physiology

Substances

  • Antineoplastic Agents
  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • Neoplasm Proteins
  • RNA, Messenger
  • RNA, Neoplasm
  • Recombinant Proteins
  • Small Molecule Libraries
  • TCF Transcription Factors
  • DNA Helicases
  • CHD1L protein, human