Phosphorylation-dependent PIH1D1 interactions define substrate specificity of the R2TP cochaperone complex

Cell Rep. 2014 Apr 10;7(1):19-26. doi: 10.1016/j.celrep.2014.03.013. Epub 2014 Mar 20.

Abstract

The R2TP cochaperone complex plays a critical role in the assembly of multisubunit machines, including small nucleolar ribonucleoproteins (snoRNPs), RNA polymerase II, and the mTORC1 and SMG1 kinase complexes, but the molecular basis of substrate recognition remains unclear. Here, we describe a phosphopeptide binding domain (PIH-N) in the PIH1D1 subunit of the R2TP complex that preferentially binds to highly acidic phosphorylated proteins. A cocrystal structure of a PIH-N domain/TEL2 phosphopeptide complex reveals a highly specific phosphopeptide recognition mechanism in which Lys57 and 64 in PIH1D1, along with a conserved DpSDD phosphopeptide motif within TEL2, are essential and sufficient for binding. Proteomic analysis of PIH1D1 interactors identified R2TP complex substrates that are recruited by the PIH-N domain in a sequence-specific and phosphorylation-dependent manner suggestive of a common mechanism of substrate recognition. We propose that protein complexes assembled by the R2TP complex are defined by phosphorylation of a specific motif and recognition by the PIH1D1 subunit.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Apoptosis Regulatory Proteins / chemistry
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism*
  • Cell Line, Tumor
  • Crystallography, X-Ray / methods*
  • HEK293 Cells
  • HSP90 Heat-Shock Proteins / chemistry
  • HSP90 Heat-Shock Proteins / genetics
  • HSP90 Heat-Shock Proteins / metabolism
  • Humans
  • Models, Molecular
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism*
  • Molecular Sequence Data
  • Multiprotein Complexes / chemistry
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism
  • Phosphorylation
  • Protein Structure, Tertiary
  • Proto-Oncogene Proteins c-ets / chemistry
  • Proto-Oncogene Proteins c-ets / metabolism
  • Sequence Homology, Amino Acid
  • Substrate Specificity

Substances

  • Apoptosis Regulatory Proteins
  • ETV7 protein, human
  • HSP90 Heat-Shock Proteins
  • Molecular Chaperones
  • Multiprotein Complexes
  • PIH1D1 protein, human
  • Proto-Oncogene Proteins c-ets

Associated data

  • PDB/4PSF
  • PDB/4PSI