Glycogen synthase kinase-3 couples AKT-dependent signaling to the regulation of p21Cip1 degradation

J Biol Chem. 2002 Mar 22;277(12):9684-9. doi: 10.1074/jbc.M106157200. Epub 2002 Jan 4.

Abstract

Signaling via the phosphoinositide 3-kinase (PI3K)/AKT pathway is crucial for the regulation of endothelial cell (EC) proliferation and survival, which involves the AKT-dependent phosphorylation of the DNA repair protein p21(Cip1) at Thr-145. Because p21(Cip1) is a short-lived protein with a high proteasomal degradation rate, we investigated the regulation of p21(Cip1) protein levels by PI3K/AKT-dependent signaling. The PI3K inhibitors Ly294002 and wortmannin reduced p21(Cip1) protein abundance in human umbilical vein EC. However, mutation of the AKT site Thr-145 into aspartate (T145D) did not increase its protein half-life. We therefore investigated whether a kinase downstream of AKT regulates p21(Cip1) protein levels. In various cell types, AKT phosphorylates and inhibits glycogen synthase kinase-3 (GSK-3). Upon serum stimulation of EC, GSK-3beta was phosphorylated at Ser-9. Site-directed mutagenesis revealed that GSK-3 in vitro phosphorylated p21(Cip1) specifically at Thr-57 within the Cdk binding domain. Overexpression of GSK-3beta decreased p21(Cip1) protein levels in EC, whereas the specific inhibition of GSK-3 with lithium chloride interfered with p21(Cip1) degradation and increased p21(Cip1) protein about 10-fold in EC and cardiac myocytes (30 mm, p < 0.001). These data indicate that GSK-3 triggers p21(Cip1) degradation. In contrast, stimulation of AKT increases p21(Cip1) via inhibitory phosphorylation of GSK-3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic / pharmacology
  • Androstadienes / pharmacology
  • Animals
  • Blotting, Western
  • Bromodeoxyuridine / pharmacology
  • COS Cells
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism*
  • Calcium-Calmodulin-Dependent Protein Kinases / physiology*
  • Cell Cycle
  • Cell Division
  • Cell Survival
  • Cells, Cultured
  • Chromones / pharmacology
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins / metabolism*
  • Dose-Response Relationship, Drug
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / enzymology*
  • Enzyme Inhibitors / pharmacology
  • Glycogen Synthase Kinase 3
  • Glycogen Synthase Kinases
  • Humans
  • Immunoblotting
  • Lithium Chloride / pharmacology
  • Morpholines / pharmacology
  • Mutagenesis, Site-Directed
  • Phosphorylation
  • Protein Binding
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-akt
  • Serine / chemistry
  • Signal Transduction
  • Threonine / chemistry
  • Time Factors
  • Transfection
  • Umbilical Veins / cytology
  • Wortmannin

Substances

  • Adjuvants, Immunologic
  • Androstadienes
  • CDKN1A protein, human
  • Chromones
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins
  • Enzyme Inhibitors
  • Morpholines
  • Proto-Oncogene Proteins
  • Threonine
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • Serine
  • Glycogen Synthase Kinases
  • AKT1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Glycogen Synthase Kinase 3
  • Bromodeoxyuridine
  • Lithium Chloride
  • Wortmannin