Protein conformational transitions coupled to binding in molecular recognition of unstructured proteins: deciphering the effect of intermolecular interactions on computational structure prediction of the p27Kip1 protein bound to the cyclin A-cyclin-dependent kinase 2 complex

Proteins. 2005 Feb 15;58(3):706-16. doi: 10.1002/prot.20351.

Abstract

The relationship between folding mechanism coupled to binding and structure prediction of the tertiary complexes is studied for the p27(Kip) (1) protein which has an intrinsically disordered unbound form and undergoes a functional folding transition during complex formation with the phosphorylated cyclin A-cyclin-dependent kinase 2 (Cdk2) binary complex. Hierarchy of p27(Kip1) structural loss determined in our earlier studies from temperature-induced Monte Carlo simulations and subsequent characterization of the transition state ensemble (TSE) for the folding reaction have shown that simultaneous ordering of the p27(Kip1) native intermolecular interface for the beta-hairpin and beta-strand secondary structure elements is critical for nucleating a rapid kinetic transition to the native tertiary complex. In the present study, we investigate the effect of forming specific intermolecular interactions on structure prediction of the p27(Kip1) tertiary complex. By constraining different secondary structure elements of p27(Kip1) in their native bound conformations and conducting multiple simulated annealing simulations, we analyze differences in the success rate of predicting the native structure of p27(Kip1) in the tertiary complex. In accordance with the nucleation-condensation mechanism, we have found that further stabilization of the native intermolecular interface for the beta-hairpin and beta-strand elements of p27(Kip1), that become ordered in the TSE, but are hardly populated in the unbound state, results in a consistent acquisition of the native bound structure. Conversely, the excessive stablization of the local secondary structure elements, which are rarely detected in the TSE, has a detrimental effect on convergence to the native bound structure.

MeSH terms

  • Cell Cycle
  • Computational Biology / methods*
  • Computer Simulation
  • Cyclin A / chemistry*
  • Cyclin-Dependent Kinase 2 / chemistry*
  • Cyclin-Dependent Kinase Inhibitor p27 / chemistry*
  • Cyclin-Dependent Kinases
  • Cyclins
  • Humans
  • Hydrogen Bonding
  • Kinetics
  • Microtubule-Associated Proteins
  • Models, Molecular
  • Models, Statistical
  • Molecular Conformation
  • Monte Carlo Method
  • Phosphorylation
  • Probability
  • Protein Binding
  • Protein Conformation
  • Protein Denaturation
  • Protein Folding
  • Protein Interaction Mapping
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Proteins / chemistry*
  • Proteomics / methods*
  • Temperature

Substances

  • Cyclin A
  • Cyclins
  • Microtubule-Associated Proteins
  • Proteins
  • Cyclin-Dependent Kinase Inhibitor p27
  • Cyclin-Dependent Kinase 2
  • Cyclin-Dependent Kinases