Deneddylation of PML/RARα reconstructs functional PML nuclear bodies via orchestrating phase separation to eradicate APL

Cell Death Differ. 2022 Aug;29(8):1654-1668. doi: 10.1038/s41418-022-00955-8. Epub 2022 Feb 22.

Abstract

Acute promyelocytic leukemia (APL) is driven by the oncoprotein PML/RARα, which destroys the architecture of PML nuclear bodies (NBs). PML NBs are critical to tumor suppression, and their disruption mediated by PML/RARα accelerates APL pathogenesis. However, the mechanisms of PML NB disruption remain elusive. Here, we reveal that the failure of NB assembly in APL results from neddylation-induced aberrant phase separation of PML/RARα. Mechanistically, PML/RARα is neddylated in the RARα moiety, and this neddylation enhances its DNA-binding ability and further impedes the phase separation of the PML moiety, consequently disrupting PML NB construction. Accordingly, deneddylation of PML/RARα restores its phase separation process to reconstruct functional NBs and activates RARα signaling, thereby suppressing PML/RARα-driven leukemogenesis. Pharmacological inhibition of neddylation by MLN4924 eradicates APL cells both in vitro and in vivo. Our work elucidates the neddylation-destroyed phase separation mechanism for PML/RARα-driven NB disruption and highlights targeting neddylation for APL eradication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Humans
  • Leukemia, Promyelocytic, Acute* / genetics
  • Leukemia, Promyelocytic, Acute* / pathology
  • Nuclear Bodies
  • Promyelocytic Leukemia Nuclear Bodies
  • Promyelocytic Leukemia Protein / genetics
  • Signal Transduction
  • Tretinoin / pharmacology

Substances

  • Promyelocytic Leukemia Protein
  • Tretinoin