In situ selectivity profiling and crystal structure of SML-8-73-1, an active site inhibitor of oncogenic K-Ras G12C

Proc Natl Acad Sci U S A. 2014 Jun 17;111(24):8895-900. doi: 10.1073/pnas.1404639111. Epub 2014 Jun 2.

Abstract

Directly targeting oncogenic V-Ki-ras2 Kirsten rat sarcoma viral oncogene homolog (K-Ras) with small-molecule inhibitors has historically been considered prohibitively challenging. Recent reports of compounds that bind directly to the K-Ras G12C mutant suggest avenues to overcome key obstacles that stand in the way of developing such compounds. We aim to target the guanine nucleotide (GN)-binding pocket because the natural contents of this pocket dictate the signaling state of K-Ras. Here, we characterize the irreversible inhibitor SML-8-73-1 (SML), which targets the GN-binding pocket of K-Ras G12C. We report a high-resolution X-ray crystal structure of G12C K-Ras bound to SML, revealing that the compound binds in a manner similar to GDP, forming a covalent linkage with Cys-12. The resulting conformation renders K-Ras in the open, inactive conformation, which is not predicted to associate productively with or activate downstream effectors. Conservation analysis of the Ras family GN-binding pocket reveals variability in the side chains surrounding the active site and adjacent regions, especially in the switch I region. This variability may enable building specificity into new iterations of Ras and other GTPase inhibitors. High-resolution in situ chemical proteomic profiling of SML confirms that SML effectively discriminates between K-Ras G12C and other cellular GTP-binding proteins. A biochemical assay provides additional evidence that SML is able to compete with millimolar concentrations of GTP and GDP for the GN-binding site.

Keywords: ActivX; CPM assay.

Publication types

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

MeSH terms

  • Acetamides / chemistry*
  • Binding Sites
  • Biotin / chemistry
  • Catalytic Domain
  • Conserved Sequence
  • Crystallography, X-Ray
  • GTP Phosphohydrolases / chemistry
  • GTP-Binding Proteins / chemistry
  • Genes, ras*
  • Guanosine Diphosphate / analogs & derivatives*
  • Guanosine Diphosphate / chemistry
  • Guanosine Triphosphate / chemistry
  • Humans
  • Ligands
  • Models, Molecular
  • Mutation
  • Phosphatidylinositol 3-Kinases / chemistry
  • Protein Binding
  • Protein Conformation
  • Proteomics
  • Signal Transduction
  • ras Proteins / antagonists & inhibitors*
  • ras Proteins / chemistry*

Substances

  • Acetamides
  • Ligands
  • SML-8-73-1
  • Guanosine Diphosphate
  • Biotin
  • Guanosine Triphosphate
  • Phosphatidylinositol 3-Kinases
  • GTP Phosphohydrolases
  • GTP-Binding Proteins
  • ras Proteins

Associated data

  • PDB/4LDJ
  • PDB/4NMM
  • PDB/4OBE