Beta2 integrin phosphorylation on Thr758 acts as a molecular switch to regulate 14-3-3 and filamin binding

Blood. 2008 Sep 1;112(5):1853-62. doi: 10.1182/blood-2007-12-127795. Epub 2008 Jun 12.

Abstract

Leukocyte integrins of the beta2 family are essential for immune cell-cell adhesion. In activated cells, beta2 integrins are phosphorylated on the cytoplasmic Thr758, leading to 14-3-3 protein recruitment to the beta2 integrin. The mutation of this phosphorylation site impairs cell adhesion, actin reorganization, and cell spreading. Thr758 is contained in a Thr triplet of beta2 that also mediates binding to filamin. Here, we investigated the binding of filamin, talin, and 14-3-3 proteins to phosphorylated and unphosphorylated beta2 integrins by biochemical methods and x-ray crystallography. 14-3-3 proteins bound only to the phosphorylated integrin cytoplasmic peptide, with a high affinity (K(d), 261 nM), whereas filamin bound only the unphosphorylated integrin cytoplasmic peptide (K(d), 0.5 mM). Phosphorylation did not regulate talin binding to beta2 directly, but 14-3-3 was able to outcompete talin for the binding to phosphorylated beta2 integrin. X-ray crystallographic data clearly explained how phosphorylation eliminated filamin binding and induced 14-3-3 protein binding. Filamin knockdown in T cells led to an increase in stimulated cell adhesion to ICAM-1-coated surfaces. Our results suggest that the phosphorylation of beta2 integrins on Thr758 acts as a molecular switch to inhibit filamin binding and allow 14-3-3 protein binding to the integrin cytoplasmic domain, thereby modulating T-cell adhesion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / chemistry
  • 14-3-3 Proteins / metabolism*
  • Amino Acid Substitution
  • Binding Sites
  • CD18 Antigens / chemistry*
  • CD18 Antigens / genetics
  • CD18 Antigens / metabolism*
  • Cell Adhesion
  • Contractile Proteins / chemistry
  • Contractile Proteins / metabolism*
  • Filamins
  • Humans
  • In Vitro Techniques
  • Intercellular Adhesion Molecule-1 / metabolism
  • Jurkat Cells
  • Microfilament Proteins / chemistry
  • Microfilament Proteins / metabolism*
  • Models, Molecular
  • Multiprotein Complexes
  • Phosphorylation
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Static Electricity
  • T-Lymphocytes / metabolism
  • Talin / metabolism
  • Threonine / chemistry

Substances

  • 14-3-3 Proteins
  • CD18 Antigens
  • Contractile Proteins
  • Filamins
  • Microfilament Proteins
  • Multiprotein Complexes
  • Recombinant Proteins
  • Talin
  • Intercellular Adhesion Molecule-1
  • Threonine

Associated data

  • PDB/2JF1
  • PDB/2V7D