α-Catenin homodimers are recruited to phosphoinositide-activated membranes to promote adhesion

J Cell Biol. 2017 Nov 6;216(11):3767-3783. doi: 10.1083/jcb.201612006. Epub 2017 Sep 5.

Abstract

A unique feature of α-catenin localized outside the cadherin-catenin complex is its capacity to form homodimers, but the subcellular localization and functions of this form of α-catenin remain incompletely understood. We identified a cadherin-free form of α-catenin that is recruited to the leading edge of migrating cells in a phosphatidylinositol 3-kinase-dependent manner. Surface plasmon resonance analysis shows that α-catenin homodimers, but not monomers, selectively bind phosphatidylinositol-3,4,5-trisphosphate-containing lipid vesicles with high affinity, where three basic residues, K488, K493, and R496, contribute to binding. Chemical-induced dimerization of α-catenin containing a synthetic dimerization domain promotes its accumulation within lamellipodia and elaboration of protrusions with extended filopodia, which are attenuated in the α-cateninKKR<3A mutant. Cells restored with a full-length, natively homodimerizing form of α-cateninKKR<3A display reduced membrane recruitment, altered epithelial sheet migrations, and weaker cell-cell adhesion compared with WT α-catenin. These findings show that α-catenin homodimers are recruited to phosphoinositide-activated membranes to promote adhesion and migration, suggesting that phosphoinositide binding may be a defining feature of α-catenin function outside the cadherin-catenin complex.

Publication types

  • Video-Audio Media
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Adhesion*
  • Cell Line, Tumor
  • Cell Membrane / metabolism*
  • Cell Movement
  • Dogs
  • Epithelial Cells / metabolism*
  • Humans
  • Madin Darby Canine Kidney Cells
  • Mutation
  • Phosphatidylinositol 3-Kinase / metabolism
  • Phosphatidylinositol Phosphates / metabolism*
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • Pseudopodia / metabolism
  • Signal Transduction
  • Time Factors
  • Transfection
  • alpha Catenin / genetics
  • alpha Catenin / metabolism*

Substances

  • Phosphatidylinositol Phosphates
  • alpha Catenin
  • phosphatidylinositol 3,4,5-triphosphate
  • Phosphatidylinositol 3-Kinase

Associated data

  • PDB/4IGG