14-3-3 proteins interact with a hybrid prenyl-phosphorylation motif to inhibit G proteins

Cell. 2013 Apr 25;153(3):640-53. doi: 10.1016/j.cell.2013.03.044.

Abstract

Signaling through G proteins normally involves conformational switching between GTP- and GDP-bound states. Several Rho GTPases are also regulated by RhoGDI binding and sequestering in the cytosol. Rnd proteins are atypical constitutively GTP-bound Rho proteins, whose regulation remains elusive. Here, we report a high-affinity 14-3-3-binding site at the C terminus of Rnd3 consisting of both the Cys241-farnesyl moiety and a Rho-associated coiled coil containing protein kinase (ROCK)-dependent Ser240 phosphorylation site. 14-3-3 binding to Rnd3 also involves phosphorylation of Ser218 by ROCK and/or Ser210 by protein kinase C (PKC). The crystal structure of a phosphorylated, farnesylated Rnd3 peptide with 14-3-3 reveals a hydrophobic groove in 14-3-3 proteins accommodating the farnesyl moiety. Functionally, 14-3-3 inhibits Rnd3-induced cell rounding by translocating it from the plasma membrane to the cytosol. Rnd1, Rnd2, and geranylgeranylated Rap1A interact similarly with 14-3-3. In contrast to the canonical GTP/GDP switch that regulates most Ras superfamily members, our results reveal an unprecedented mechanism for G protein inhibition by 14-3-3 proteins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / chemistry*
  • 14-3-3 Proteins / metabolism*
  • Amino Acid Sequence
  • Animals
  • COS Cells
  • Cell Membrane / metabolism
  • Chlorocebus aethiops
  • Crystallography, X-Ray
  • Cytosol / metabolism
  • Humans
  • Models, Molecular
  • Molecular Sequence Data
  • Phosphorylation
  • Prenylation
  • Protein Interaction Domains and Motifs
  • rho GTP-Binding Proteins / chemistry*
  • rho GTP-Binding Proteins / genetics
  • rho GTP-Binding Proteins / metabolism*

Substances

  • 14-3-3 Proteins
  • YWHAZ protein, human
  • RND3 protein, human
  • rho GTP-Binding Proteins

Associated data

  • PDB/4BG6