PRMT1 promotes the tumor suppressor function of p14ARF and is indicative for pancreatic cancer prognosis

EMBO J. 2021 Jul 1;40(13):e106777. doi: 10.15252/embj.2020106777. Epub 2021 May 17.

Abstract

The p14ARF protein is a well-known regulator of p53-dependent and p53-independent tumor-suppressive activities. In unstressed cells, p14ARF is predominantly sequestered in the nucleoli, bound to its nucleolar interaction partner NPM. Upon genotoxic stress, p14ARF undergoes an immediate redistribution to the nucleo- and cytoplasm, where it promotes activation of cell cycle arrest and apoptosis. Here, we identify p14ARF as a novel interaction partner and substrate of PRMT1 (protein arginine methyltransferase 1). PRMT1 methylates several arginine residues in the C-terminal nuclear/nucleolar localization sequence (NLS/NoLS) of p14ARF . In the absence of cellular stress, these arginines are crucial for nucleolar localization of p14ARF . Genotoxic stress causes augmented interaction between PRMT1 and p14ARF , accompanied by arginine methylation of p14ARF . PRMT1-dependent NLS/NoLS methylation promotes the release of p14ARF from NPM and nucleolar sequestration, subsequently leading to p53-independent apoptosis. This PRMT1-p14ARF cooperation is cancer-relevant and indicative for PDAC (pancreatic ductal adenocarcinoma) prognosis and chemotherapy response of pancreatic tumor cells. Our data reveal that PRMT1-mediated arginine methylation is an important trigger for p14ARF 's stress-induced tumor-suppressive function.

Keywords: apoptosis; arginine methylation; pancreatic cancer; post-translational modification; tumor suppression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / physiology
  • Cell Cycle / physiology
  • Cell Line
  • Cell Line, Tumor
  • Cell Nucleolus / metabolism
  • Cell Nucleus / metabolism
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Neoplasm Proteins / metabolism
  • Nuclear Proteins / metabolism
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology
  • Prognosis
  • Protein-Arginine N-Methyltransferases / metabolism*
  • Repressor Proteins / metabolism*
  • Sf9 Cells
  • Tumor Suppressor Protein p14ARF / metabolism*
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Neoplasm Proteins
  • Nuclear Proteins
  • Repressor Proteins
  • Tumor Suppressor Protein p14ARF
  • Tumor Suppressor Protein p53
  • PRMT1 protein, human
  • Protein-Arginine N-Methyltransferases