β-Arrestin1 and Signal-transducing Adaptor Molecule 1 (STAM1) Cooperate to Promote Focal Adhesion Kinase Autophosphorylation and Chemotaxis via the Chemokine Receptor CXCR4

J Biol Chem. 2016 Dec 9;291(50):26083-26097. doi: 10.1074/jbc.M116.757138. Epub 2016 Oct 27.

Abstract

The chemokine receptor CXCR4 and its chemokine ligand CXCL12 mediate directed cell migration during organogenesis, immune responses, and metastatic disease. However, the mechanisms governing CXCL12/CXCR4-dependent chemotaxis remain poorly understood. Here, we show that the β-arrestin1·signal-transducing adaptor molecule 1 (STAM1) complex, initially identified to govern lysosomal trafficking of CXCR4, also mediates CXCR4-dependent chemotaxis. Expression of minigene fragments from β-arrestin1 or STAM1, known to disrupt the β-arrestin1·STAM1 complex, and RNAi against β-arrestin1 or STAM1, attenuates CXCL12-induced chemotaxis. The β-arrestin1·STAM1 complex is necessary for promoting autophosphorylation of focal adhesion kinase (FAK). FAK is necessary for CXCL12-induced chemotaxis and associates with and localizes with β-arrestin1 and STAM1 in a CXCL12-dependent manner. Our data reveal previously unknown roles in CXCR4-dependent chemotaxis for β-arrestin1 and STAM1, which we propose act in concert to regulate FAK signaling. The β-arrestin1·STAM1 complex is a promising target for blocking CXCR4-promoted FAK autophosphorylation and chemotaxis.

Keywords: C-X-C chemokine receptor type 4 (CXCR-4); CXCL12; G protein-coupled receptor (GPCR); PTK2 protein tyrosine kinase 2 (PTK2) (focal adhesion kinase) (FAK); STAM; chemokine; chemotaxis; β-arrestin.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Chemokine CXCL12 / genetics
  • Chemokine CXCL12 / metabolism
  • Chemotaxis / physiology*
  • Endosomal Sorting Complexes Required for Transport / genetics
  • Endosomal Sorting Complexes Required for Transport / metabolism*
  • Focal Adhesion Kinase 1 / genetics
  • Focal Adhesion Kinase 1 / metabolism*
  • HeLa Cells
  • Humans
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism*
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Phosphorylation / physiology
  • Receptors, CXCR4 / genetics
  • Receptors, CXCR4 / metabolism*
  • Signal Transduction / physiology
  • beta-Arrestin 1 / genetics
  • beta-Arrestin 1 / metabolism*

Substances

  • ARRB1 protein, human
  • Adaptor Proteins, Signal Transducing
  • CXCL12 protein, human
  • CXCR4 protein, human
  • Chemokine CXCL12
  • Endosomal Sorting Complexes Required for Transport
  • Multiprotein Complexes
  • Phosphoproteins
  • Receptors, CXCR4
  • STAM protein, human
  • beta-Arrestin 1
  • Focal Adhesion Kinase 1
  • PTK2 protein, human