The induction of microRNA-16 in colon cancer cells by protein arginine deiminase inhibition causes a p53-dependent cell cycle arrest

PLoS One. 2013;8(1):e53791. doi: 10.1371/journal.pone.0053791. Epub 2013 Jan 7.

Abstract

Protein Arginine Deiminases (PADs) catalyze the post-translational conversion of peptidyl-Arginine to peptidyl-Citrulline in a calcium-dependent, irreversible reaction. Evidence is emerging that PADs play a role in carcinogenesis. To determine the cancer-associated functional implications of PADs, we designed a small molecule PAD inhibitor (called Chor-amidine or Cl-amidine), and tested the impact of this drug on the cell cycle. Data derived from experiments in colon cancer cells indicate that Cl-amidine causes a G1 arrest, and that this was p53-dependent. In a separate set of experiments, we found that Cl-amidine caused a significant increase in microRNA-16 (miRNA-16), and that this increase was also p53-dependent. Because miRNA-16 is a putative tumor suppressor miRNA, and others have found that miRNA-16 suppresses proliferation, we hypothesized that the p53-dependent G1 arrest associated with PAD inhibition was, in turn, dependent on miRNA-16 expression. Results are consistent with this hypothesis. As well, we found the G1 arrest is at least in part due to the ability of Cl-amidine-mediated expression of miRNA-16 to suppress its' G1-associated targets: cyclins D1, D2, D3, E1, and cdk6. Our study sheds light into the mechanisms by which PAD inhibition can protect against or treat colon cancer.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amidines / chemical synthesis
  • Amidines / pharmacology*
  • Cell Cycle Checkpoints / drug effects*
  • Cell Cycle Checkpoints / genetics
  • Cell Line, Tumor
  • Colonic Neoplasms / drug therapy
  • Colonic Neoplasms / genetics
  • Colonic Neoplasms / metabolism
  • Colonic Neoplasms / pathology
  • Cyclin D / genetics
  • Cyclin D / metabolism
  • Cyclin E / genetics
  • Cyclin E / metabolism
  • Cyclin-Dependent Kinase 6 / genetics
  • Cyclin-Dependent Kinase 6 / metabolism
  • Enzyme Inhibitors / chemical synthesis
  • Enzyme Inhibitors / pharmacology*
  • G1 Phase / drug effects
  • G1 Phase / genetics
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Hydrolases / antagonists & inhibitors*
  • Hydrolases / genetics
  • Hydrolases / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • Protein-Arginine Deiminases
  • Signal Transduction
  • Tumor Suppressor Protein p53 / agonists*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Amidines
  • Cyclin D
  • Cyclin E
  • Enzyme Inhibitors
  • MIRN16 microRNA, human
  • MicroRNAs
  • Protein Isoforms
  • Tumor Suppressor Protein p53
  • CDK6 protein, human
  • Cyclin-Dependent Kinase 6
  • Hydrolases
  • Protein-Arginine Deiminases