Phosphorylation of human enhancer filamentation 1 (HEF1) stimulates interaction with Polo-like kinase 1 leading to HEF1 localization to focal adhesions

J Biol Chem. 2018 Jan 19;293(3):847-862. doi: 10.1074/jbc.M117.802587. Epub 2017 Nov 30.

Abstract

Elevated expression of human enhancer filamentation 1 (HEF1; also known as NEDD9 or Cas-L) is an essential stimulus for the metastatic process of various solid tumors. This process requires HEF1 localization to focal adhesions (FAs). Although the association of HEF1 with FAs is considered to play a role in cancer cell migration, the mechanism targeting HEF1 to FAs remains unclear. Moreover, up-regulation of Polo-like kinase 1 (Plk1) positively correlates with human cancer metastasis, yet how Plk1 deregulation promotes metastasis remains elusive. Here, we report that casein kinase 1δ (CK1δ) phosphorylates HEF1 at Ser-780 and Thr-804 and that these phosphorylation events promote a physical interaction between Plk1 and HEF1. We found that this interaction is critical for HEF1 translocation to FAs and for inducing migration of HeLa cells. Plk1-docking phosphoepitopes were mapped/confirmed in HEF1 by various methods, including X-ray crystallography, and mutated for functional analysis in HeLa cells. In summary, our results reveal the role of a phosphorylation-dependent HEF1-Plk1 complex in HEF1 translocation to FAs to induce cell migration. Our findings provide critical mechanistic insights into the HEF1-Plk1 complex-dependent localization of HEF1 to FAs underlying the metastatic process and may therefore contribute to the development of new cancer therapies.

Keywords: HEF1 pSer-780; HEF1 pThr-804; HEF1 translocation; HEF1-Plk1 complex; Plk1; cell migration; focal adhesion; phosphorylation; protein targeting; protein-protein interaction; proton transport; serine/threonine protein kinase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Line
  • Cell Proliferation / genetics
  • Cell Proliferation / physiology
  • Focal Adhesions / genetics
  • Focal Adhesions / metabolism*
  • HeLa Cells
  • Humans
  • Immunoblotting
  • Immunoprecipitation
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Phosphorylation / genetics
  • Phosphorylation / physiology
  • Polo-Like Kinase 1
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Cell Cycle Proteins
  • NEDD9 protein, human
  • Phosphoproteins
  • Proto-Oncogene Proteins
  • Protein Serine-Threonine Kinases

Associated data

  • PDB/5X3S
  • PDB/3HIK