The RAX/PACT-PKR stress response pathway promotes p53 sumoylation and activation, leading to G₁ arrest

Cell Cycle. 2012 Jan 15;11(2):407-17. doi: 10.4161/cc.11.2.18999. Epub 2012 Jan 15.

Abstract

Cellular stresses, including growth factor deprivation, inflammatory cytokines or viral infection promote RAX/PACT-dependent activation of the double-stranded RNA-dependent protein kinase, PKR, to phosphorylate eIF2α, resulting in translation inhibition and apoptosis. In addition, PKR has been reported to regulate p53, STAT1 and NFκB. Here, we report that RAX/PACT interacts with the SUMO E2 ligase Ubc9 to stimulate p53-Ubc9 association and reversible p53 sumoylation on lysine 386. In addition, expression of RAX/PACT in a variety of cell lines promotes p53 stability and activity to increase p53 target gene expression. Significantly, while the expression of RAX/PACT, PKR or p53 alone has little effect on the cell cycle of p53-null H1299 cells, co-expression of p53 with either RAX/PACT or PKR promotes a 25-35% increase of cells in G₁. In contrast, co-expression of RAX/PACT with the sumoylation-deficient p53(K386R) mutant or with the desumoylase SENP1 fails to induce such a G₁ arrest. Furthermore, co-expression of p53, RAX/PACT and the dominantnegative PKR(K296R) mutant inhibits RAX/PACT-induced, p53-dependent G₁ growth arrest and expression of RAX/PACT in pkr(+/+) but not pkr(-/-) MEF cells promotes p53 and p21 expression following gamma irradiation. Significantly, p53 stability is decreased in cells with reduced RAX/PACT or PKR following doxorubicin treatment, and expression of exogenous RAX/ PACT promotes phosphorylation of wild-type but not p53(K386R) on serine 392. Collectively, results indicate that, in response to stress, the RAX/PACT-PKR signaling pathway may inhibit p53 protein turnover by a sumoylation-dependent mechanism with promotion of p53 phosphorylation and translational activation leading to G₁ cell cycle arrest.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line, Tumor
  • Eukaryotic Initiation Factor-2 / metabolism
  • Eye Proteins / metabolism*
  • G1 Phase Cell Cycle Checkpoints*
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Homeodomain Proteins / metabolism*
  • Humans
  • Phosphorylation
  • Protein Binding
  • Protein Biosynthesis
  • Protein Processing, Post-Translational
  • RNA-Binding Proteins / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction
  • Stress, Physiological
  • Sumoylation
  • Transcription Factors / metabolism*
  • Transcriptional Activation
  • Tumor Suppressor Protein p53 / metabolism*
  • Two-Hybrid System Techniques
  • Ubiquitin-Conjugating Enzymes / metabolism
  • eIF-2 Kinase / metabolism*

Substances

  • Eukaryotic Initiation Factor-2
  • Eye Proteins
  • Homeodomain Proteins
  • PRKRA protein, human
  • RAX protein, human
  • RNA-Binding Proteins
  • TP53 protein, human
  • Transcription Factors
  • Tumor Suppressor Protein p53
  • Ubiquitin-Conjugating Enzymes
  • eIF-2 Kinase
  • ubiquitin-conjugating enzyme UBC9