GRWD1 negatively regulates p53 via the RPL11-MDM2 pathway and promotes tumorigenesis

EMBO Rep. 2017 Jan;18(1):123-137. doi: 10.15252/embr.201642444. Epub 2016 Nov 17.

Abstract

The ribosomal protein L11 (RPL11) binds and inhibits the MDM2 ubiquitin ligase, thereby promoting p53 stability. Thus, RPL11 acts as a tumor suppressor. Here, we show that GRWD1 (glutamate-rich WD40 repeat containing 1) physically and functionally interacts with RPL11. GRWD1 is localized to nucleoli and is released into the nucleoplasm upon nucleolar stress. Silencing of GRWD1 increases p53 induction by nucleolar stress, whereas overexpression of GRWD1 reduces p53 induction. Furthermore, GRWD1 overexpression competitively inhibits the RPL11-MDM2 interaction and alleviates RPL11-mediated suppression of MDM2 ubiquitin ligase activity toward p53. These effects are mediated by the N-terminal region of GRWD1, including the acidic domain. Finally, we show that GRWD1 overexpression in combination with HPV16 E7 and activated KRAS confers anchorage-independent growth and tumorigenic capacity on normal human fibroblasts. Consistent with this, GRWD1 overexpression is associated with poor prognosis in cancer patients. Taken together, our results suggest that GRWD1 is a novel negative regulator of p53 and a potential oncogene.

Keywords: GRWD1; nucleolar stress; p53/RPL11; tumorigenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carrier Proteins / chemistry
  • Carrier Proteins / metabolism*
  • Cell Line, Tumor
  • Cell Transformation, Neoplastic / genetics*
  • Cell Transformation, Neoplastic / metabolism*
  • Cell Transformation, Viral
  • Disease Models, Animal
  • Female
  • Gene Expression
  • Gene Expression Regulation, Neoplastic*
  • Gene Silencing
  • Genes, ras
  • Heterografts
  • Humans
  • Mice
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Neoplasms / mortality
  • Neoplasms / pathology
  • Prognosis
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Protein Stability
  • Proto-Oncogene Proteins c-mdm2 / metabolism*
  • Ribosomal Proteins / metabolism*
  • Signal Transduction*
  • Stress, Physiological
  • Tumor Suppressor Protein p53 / genetics*
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Carrier Proteins
  • GRWD1 protein, human
  • Ribosomal Proteins
  • Tumor Suppressor Protein p53
  • ribosomal protein L11
  • Proto-Oncogene Proteins c-mdm2