USP1 links platinum resistance to cancer cell dissemination by regulating Snail stability

Sci Adv. 2019 May 8;5(5):eaav3235. doi: 10.1126/sciadv.aav3235. eCollection 2019 May.

Abstract

Resistance to platinum-based chemotherapy is a common event in patients with cancer, generally associated with tumor dissemination and metastasis. Whether platinum treatment per se activates molecular pathways linked to tumor spreading is not known. Here, we report that the ubiquitin-specific protease 1 (USP1) mediates ovarian cancer cell resistance to platinum, by regulating the stability of Snail, which, in turn, promotes tumor dissemination. At the molecular level, we observed that upon platinum treatment, USP1 is phosphorylated by ATM and ATR and binds to Snail. Then, USP1 de-ubiquitinates and stabilizes Snail expression, conferring resistance to platinum, increased stem cell-like features, and metastatic ability. Consistently, knockout or pharmacological inhibition of USP1 increased platinum sensitivity and decreased metastatic dissemination in a Snail-dependent manner. Our findings identify Snail as a USP1 target and open the way to a novel strategy to overcome platinum resistance and more successfully treat patients with ovarian cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Ataxia Telangiectasia Mutated Proteins / metabolism
  • Cell Line, Tumor
  • Coordination Complexes / pharmacology*
  • Coordination Complexes / therapeutic use
  • Drug Resistance, Neoplasm
  • Female
  • Gene Editing
  • Humans
  • Mice
  • Mice, Nude
  • Ovarian Neoplasms / drug therapy
  • Ovarian Neoplasms / pathology
  • Phosphorylation
  • Platinum / chemistry*
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Snail Family Transcription Factors / antagonists & inhibitors
  • Snail Family Transcription Factors / genetics
  • Snail Family Transcription Factors / metabolism*
  • Ubiquitin-Specific Proteases / antagonists & inhibitors
  • Ubiquitin-Specific Proteases / genetics
  • Ubiquitin-Specific Proteases / metabolism*
  • Ubiquitination
  • Xenograft Model Antitumor Assays

Substances

  • Coordination Complexes
  • RNA, Small Interfering
  • SNAI1 protein, human
  • Snail Family Transcription Factors
  • Platinum
  • Ataxia Telangiectasia Mutated Proteins
  • USP1 protein, human
  • Ubiquitin-Specific Proteases