Loss of USP28-mediated BRAF degradation drives resistance to RAF cancer therapies

J Exp Med. 2018 Jul 2;215(7):1913-1928. doi: 10.1084/jem.20171960. Epub 2018 Jun 7.

Abstract

RAF kinase inhibitors are clinically active in patients with BRAF (V600E) mutant melanoma. However, rarely do tumors regress completely, with the majority of responses being short-lived. This is partially mediated through the loss of negative feedback loops after MAPK inhibition and reactivation of upstream signaling. Here, we demonstrate that the deubiquitinating enzyme USP28 functions through a feedback loop to destabilize RAF family members. Loss of USP28 stabilizes BRAF enhancing downstream MAPK activation and promotes resistance to RAF inhibitor therapy in culture and in vivo models. Importantly, we demonstrate that USP28 is deleted in a proportion of melanoma patients and may act as a biomarker for response to BRAF inhibitor therapy in patients. Furthermore, we identify Rigosertib as a possible therapeutic strategy for USP28-depleted tumors. Our results show that loss of USP28 enhances MAPK activity through the stabilization of RAF family members and is a key factor in BRAF inhibitor resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Cell Line, Tumor
  • Down-Regulation
  • Drug Resistance, Neoplasm*
  • F-Box-WD Repeat-Containing Protein 7 / metabolism
  • Gene Deletion
  • Glycine / analogs & derivatives
  • Glycine / pharmacology
  • Glycine / therapeutic use
  • HEK293 Cells
  • Humans
  • MAP Kinase Signaling System
  • Melanoma / drug therapy*
  • Melanoma / metabolism*
  • Melanoma / pathology
  • Mice
  • Prognosis
  • Protein Stability
  • Proteolysis*
  • Proto-Oncogene Proteins B-raf / metabolism*
  • Sulfones / pharmacology
  • Sulfones / therapeutic use
  • Ubiquitin Thiolesterase / deficiency*
  • Vemurafenib / pharmacology
  • Vemurafenib / therapeutic use

Substances

  • F-Box-WD Repeat-Containing Protein 7
  • FBXW7 protein, human
  • Sulfones
  • USP28 protein, human
  • Vemurafenib
  • ON 01910
  • Proto-Oncogene Proteins B-raf
  • Ubiquitin Thiolesterase
  • Glycine