LLY-507, a Cell-active, Potent, and Selective Inhibitor of Protein-lysine Methyltransferase SMYD2

J Biol Chem. 2015 May 29;290(22):13641-53. doi: 10.1074/jbc.M114.626861. Epub 2015 Mar 30.

Abstract

SMYD2 is a lysine methyltransferase that catalyzes the monomethylation of several protein substrates including p53. SMYD2 is overexpressed in a significant percentage of esophageal squamous primary carcinomas, and that overexpression correlates with poor patient survival. However, the mechanism(s) by which SMYD2 promotes oncogenesis is not understood. A small molecule probe for SMYD2 would allow for the pharmacological dissection of this biology. In this report, we disclose LLY-507, a cell-active, potent small molecule inhibitor of SMYD2. LLY-507 is >100-fold selective for SMYD2 over a broad range of methyltransferase and non-methyltransferase targets. A 1.63-Å resolution crystal structure of SMYD2 in complex with LLY-507 shows the inhibitor binding in the substrate peptide binding pocket. LLY-507 is active in cells as measured by reduction of SMYD2-induced monomethylation of p53 Lys(370) at submicromolar concentrations. We used LLY-507 to further test other potential roles of SMYD2. Mass spectrometry-based proteomics showed that cellular global histone methylation levels were not significantly affected by SMYD2 inhibition with LLY-507, and subcellular fractionation studies indicate that SMYD2 is primarily cytoplasmic, suggesting that SMYD2 targets a very small subset of histones at specific chromatin loci and/or non-histone substrates. Breast and liver cancers were identified through in silico data mining as tumor types that display amplification and/or overexpression of SMYD2. LLY-507 inhibited the proliferation of several esophageal, liver, and breast cancer cell lines in a dose-dependent manner. These findings suggest that LLY-507 serves as a valuable chemical probe to aid in the dissection of SMYD2 function in cancer and other biological processes.

Keywords: SMYD2; cancer biology; chemical probe; crystal structure; enzyme inhibitor; epigenetics; methyltransferase; protein methylation.

Publication types

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

MeSH terms

  • Antineoplastic Agents / chemistry*
  • Benzamides / chemistry*
  • Cell Line, Tumor
  • Cell Proliferation
  • Chromatin / chemistry
  • Computational Biology
  • Crystallization
  • Crystallography, X-Ray
  • Dose-Response Relationship, Drug
  • Drug Screening Assays, Antitumor
  • Enzyme Inhibitors / chemistry*
  • Epigenesis, Genetic
  • Histone-Lysine N-Methyltransferase / antagonists & inhibitors*
  • Histones / chemistry
  • Humans
  • Mass Spectrometry
  • Neoplasms / drug therapy
  • Neoplasms / enzymology*
  • Peptides / chemistry
  • Protein Denaturation
  • Proteomics
  • Pyrrolidines / chemistry*
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Antineoplastic Agents
  • Benzamides
  • Chromatin
  • Enzyme Inhibitors
  • Histones
  • LLY-507
  • Peptides
  • Pyrrolidines
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Histone-Lysine N-Methyltransferase
  • SMYD2 protein, human

Associated data

  • PDB/4WUY