Small-molecule inhibitors of USP1 target ID1 degradation in leukemic cells

Mol Cancer Ther. 2013 Dec;12(12):2651-62. doi: 10.1158/1535-7163.MCT-13-0103-T. Epub 2013 Oct 15.

Abstract

Inhibitor of DNA binding 1 (ID1) transcription factor is essential for the proliferation and progression of many cancer types, including leukemia. However, the ID1 protein has not yet been therapeutically targeted in leukemia. ID1 is normally polyubiquitinated and degraded by the proteasome. Recently, it has been shown that USP1, a ubiquitin-specific protease, deubiquitinates ID1 and rescues it from proteasome degradation. Inhibition of USP1 therefore offers a new avenue to target ID1 in cancer. Here, using a ubiquitin-rhodamine-based high-throughput screening, we identified small-molecule inhibitors of USP1 and investigated their therapeutic potential for leukemia. These inhibitors blocked the deubiquitinating enzyme activity of USP1 in vitro in a dose-dependent manner with an IC50 in the high nanomolar range. USP1 inhibitors promoted the degradation of ID1 and, concurrently, inhibited the growth of leukemic cell lines in a dose-dependent manner. A known USP1 inhibitor, pimozide, also promoted ID1 degradation and inhibited growth of leukemic cells. In addition, the growth of primary acute myelogenous leukemia (AML) patient-derived leukemic cells was inhibited by a USP1 inhibitor. Collectively, these results indicate that the novel small-molecule inhibitors of USP1 promote ID1 degradation and are cytotoxic to leukemic cells. The identification of USP1 inhibitors therefore opens up a new approach for leukemia therapy.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / metabolism
  • Antineoplastic Agents / pharmacology
  • Arabidopsis Proteins / antagonists & inhibitors*
  • Arabidopsis Proteins / metabolism
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Drug Screening Assays, Antitumor
  • Enzyme Activation / drug effects
  • Fanconi Anemia Complementation Group D2 Protein / metabolism
  • High-Throughput Screening Assays
  • Homologous Recombination / drug effects
  • Humans
  • Inhibitor of Differentiation Protein 1 / metabolism*
  • Inhibitory Concentration 50
  • Leukemia / genetics
  • Leukemia / metabolism*
  • Mice
  • Pimozide / pharmacology
  • Protease Inhibitors / chemistry
  • Protease Inhibitors / metabolism
  • Protease Inhibitors / pharmacology*
  • Protein Binding
  • Proteolysis / drug effects
  • Ubiquitin-Specific Proteases / antagonists & inhibitors*
  • Ubiquitin-Specific Proteases / metabolism
  • Ubiquitination / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Arabidopsis Proteins
  • Fanconi Anemia Complementation Group D2 Protein
  • Inhibitor of Differentiation Protein 1
  • Protease Inhibitors
  • Pimozide
  • USP1 protein, human
  • Ubiquitin-Specific Proteases