Specific beta1 integrin site selectively regulates Akt/protein kinase B signaling via local activation of protein phosphatase 2A

J Biol Chem. 2003 May 16;278(20):18671-81. doi: 10.1074/jbc.M300879200. Epub 2003 Mar 11.

Abstract

Integrin transmembrane receptors generate multiple signals, but how they mediate specific signaling is not clear. Here we test the hypothesis that particular sequences along the beta(1) integrin cytoplasmic domain may exist that are intimately related to specific integrin-mediated signaling pathways. Using systematic alanine mutagenesis of amino acids conserved between different beta integrin cytoplasmic domains, we identified the tryptophan residue at position 775 of human beta(1) integrin as specific and necessary for integrin-mediated protein kinase B/Akt survival signaling. Stable expression of a beta(1) integrin mutated at this amino acid in GD25 beta(1)-null cells resulted in reduction of Akt phosphorylation at both Ser(473) and Thr(308) activation sites. As a consequence, the cells were substantially more sensitive to serum starvation-induced apoptosis when compared with cells expressing wild type beta(1) integrin. This inactivation of Akt resulted from increased dephosphorylation by a localized active population of protein phosphatase 2A. Both Akt and protein phosphatase 2A were present in beta(1) integrin-organized cytoplasmic complexes, but the activity of this phosphatase was 2.5 times higher in the complexes organized by the mutant integrin. The mutation of Trp(775) specifically affected Akt signaling, without effects on other integrin-activated pathways including phosphoinositide 3-kinase, MAPK, JNK, and p38 nor did it influence activation of the integrin-responsive kinases focal adhesion kinase and Src. The identification of Trp(775) as a specific site for integrin-mediated Akt signaling supports the concept of specificity of signaling along the integrin cytoplasmic domain.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Apoptosis
  • Base Sequence
  • Binding Sites
  • Cell Line
  • Cytoplasm / metabolism
  • DNA, Complementary / metabolism
  • Flow Cytometry
  • Humans
  • Immunoblotting
  • Integrin beta1 / chemistry*
  • Integrin beta1 / metabolism
  • Integrins / metabolism
  • Mice
  • Microscopy, Fluorescence
  • Mitogen-Activated Protein Kinases / metabolism
  • Molecular Sequence Data
  • Mutation
  • Phosphoprotein Phosphatases / metabolism*
  • Phosphorylation
  • Precipitin Tests
  • Protein Binding
  • Protein Phosphatase 2
  • Protein Serine-Threonine Kinases*
  • Protein Structure, Tertiary
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-akt
  • Rats
  • Signal Transduction
  • Time Factors
  • Transfection
  • p38 Mitogen-Activated Protein Kinases

Substances

  • DNA, Complementary
  • Integrin beta1
  • Integrins
  • Proto-Oncogene Proteins
  • AKT1 protein, human
  • Akt1 protein, rat
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Phosphoprotein Phosphatases
  • Protein Phosphatase 2