Structural Basis of Ribosomal S6 Kinase 1 (RSK1) Inhibition by S100B Protein: MODULATION OF THE EXTRACELLULAR SIGNAL-REGULATED KINASE (ERK) SIGNALING CASCADE IN A CALCIUM-DEPENDENT WAY

J Biol Chem. 2016 Jan 1;291(1):11-27. doi: 10.1074/jbc.M115.684928. Epub 2015 Nov 2.

Abstract

Mitogen-activated protein kinases (MAPK) promote MAPK-activated protein kinase activation. In the MAPK pathway responsible for cell growth, ERK2 initiates the first phosphorylation event on RSK1, which is inhibited by Ca(2+)-binding S100 proteins in malignant melanomas. Here, we present a detailed in vitro biochemical and structural characterization of the S100B-RSK1 interaction. The Ca(2+)-dependent binding of S100B to the calcium/calmodulin-dependent protein kinase (CaMK)-type domain of RSK1 is reminiscent of the better known binding of calmodulin to CaMKII. Although S100B-RSK1 and the calmodulin-CAMKII system are clearly distinct functionally, they demonstrate how unrelated intracellular Ca(2+)-binding proteins could influence the activity of the CaMK domain-containing protein kinases. Our crystallographic, small angle x-ray scattering, and NMR analysis revealed that S100B forms a "fuzzy" complex with RSK1 peptide ligands. Based on fast-kinetics experiments, we conclude that the binding involves both conformation selection and induced fit steps. Knowledge of the structural basis of this interaction could facilitate therapeutic targeting of melanomas.

Keywords: RSK; S100 proteins; calcium; crystal structure; extracellular-signal-regulated kinase (ERK); kinetics; melanoma; mitogen-activated protein kinase (MAPK); nuclear magnetic resonance (NMR); small-angle X-ray scattering (SAXS).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Calcium / metabolism*
  • Crystallography, X-Ray
  • Enzyme Activation
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Fluorescence Polarization
  • Kinetics
  • MAP Kinase Signaling System*
  • Models, Molecular
  • Molecular Sequence Data
  • Protein Binding
  • Protein Structure, Tertiary
  • Ribosomal Protein S6 Kinases, 90-kDa / antagonists & inhibitors*
  • Ribosomal Protein S6 Kinases, 90-kDa / chemistry*
  • Ribosomal Protein S6 Kinases, 90-kDa / metabolism
  • S100 Calcium Binding Protein beta Subunit / chemistry
  • S100 Calcium Binding Protein beta Subunit / metabolism*
  • Solutions
  • Structure-Activity Relationship
  • Tryptophan / metabolism

Substances

  • S100 Calcium Binding Protein beta Subunit
  • Solutions
  • Tryptophan
  • Ribosomal Protein S6 Kinases, 90-kDa
  • Extracellular Signal-Regulated MAP Kinases
  • Calcium

Associated data

  • PDB/5CSF
  • PDB/5CSI
  • PDB/5CSJ
  • PDB/5CSN