Enzymatic Analysis of PTEN Ubiquitylation by WWP2 and NEDD4-1 E3 Ligases

Biochemistry. 2016 Jul 5;55(26):3658-66. doi: 10.1021/acs.biochem.6b00448. Epub 2016 Jun 22.

Abstract

PTEN is a lipid phosphatase that converts phosphatidylinositol 3,4,5-phosphate (PIP3) to phosphatidylinositol 4,5-phosphate (PIP2) and plays a critical role in the regulation of tumor growth. PTEN is subject to regulation by a variety of post-translational modifications, including phosphorylation on a C-terminal cluster of four Ser/Thr residues (380, 382, 383, and 385) and ubiquitylation by various E3 ligases, including NEDD4-1 and WWP2. It has previously been shown that C-terminal phosphorylation of PTEN can increase its cellular half-life. Using in vitro ubiquitin transfer assays, we show that WWP2 is more active than NEDD4-1 in ubiquitylating unphosphorylated PTEN. The mapping of ubiquitylation sites in PTEN by mass spectrometry showed that both NEDD4-1 and WWP2 can target a broad range of Lys residues in PTEN, although NEDD4-1 versus WWP2 showed a stronger preference for ubiquitylating PTEN's C2 domain. Whereas tetraphosphorylation of PTEN did not significantly affect its ubiquitylation by NEDD4-1, it inhibited PTEN ubiquitylation by WWP2. Single-turnover and pull-down experiments suggested that tetraphosphorylation of PTEN appears to weaken its interaction with WWP2. These studies reveal how the PTEN E3 ligases WWP2 and NEDD4-1 exhibit distinctive properties in Lys selectivity and sensitivity to PTEN phosphorylation. Our findings also provide a molecular mechanism for the connection between PTEN Ser/Thr phosphorylation and PTEN's cellular stability.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Chromatography, Liquid
  • Endosomal Sorting Complexes Required for Transport / metabolism*
  • Humans
  • Immunoprecipitation
  • Nedd4 Ubiquitin Protein Ligases
  • PTEN Phosphohydrolase / metabolism*
  • Phosphorylation
  • Protein Processing, Post-Translational
  • Tandem Mass Spectrometry
  • Ubiquitin / metabolism*
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination
  • X-Linked Inhibitor of Apoptosis Protein / metabolism*

Substances

  • Endosomal Sorting Complexes Required for Transport
  • Ubiquitin
  • X-Linked Inhibitor of Apoptosis Protein
  • XIAP protein, human
  • Nedd4 Ubiquitin Protein Ligases
  • Nedd4 protein, human
  • WWP2 protein, human
  • Ubiquitin-Protein Ligases
  • PTEN Phosphohydrolase
  • PTEN protein, human