Targeting deubiquitinase activity with a novel small-molecule inhibitor as therapy for B-cell malignancies

Blood. 2015 Jun 4;125(23):3588-97. doi: 10.1182/blood-2014-10-605584. Epub 2015 Mar 26.

Abstract

Usp9x was recently shown to be highly expressed in myeloma patients with short progression-free survival and is proposed to enhance stability of the survival protein Mcl-1. In this study, we found that the partially selective Usp9x deubiquitinase inhibitor WP1130 induced apoptosis and reduced Mcl-1 protein levels. However, short hairpin RNA-mediated knockdown (KD) of Usp9x in myeloma cells resulted in transient induction of apoptosis, followed by a sustained reduction in cell growth. A compensatory upregulation of Usp24, a deubiquitinase closely related to Usp9x, in Usp9x KD cells was noted. Direct Usp24 KD resulted in marked induction of myeloma cell death that was associated with a reduction of Mcl-1. Usp24 was found to sustain myeloma cell survival and Mcl-1 regulation in the absence of Usp9x. Both Usp9x and Usp24 were expressed and activated in primary myeloma cells whereas Usp24 protein overexpression was noted in some patients with drug-refractory myeloma and other B-cell malignancies. Furthermore, we improved the drug-like properties of WP1130 and demonstrated that the novel compound EOAI3402143 dose-dependently inhibited Usp9x and Usp24 activity, increased tumor cell apoptosis, and fully blocked or regressed myeloma tumors in mice. We conclude that small-molecule Usp9x/Usp24 inhibitors may have therapeutic activity in myeloma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Apoptosis / genetics
  • Cell Line, Tumor
  • Cyanoacrylates / pharmacology*
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology*
  • Female
  • Gene Expression Regulation, Enzymologic / drug effects
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Lymphoma, Mantle-Cell / drug therapy*
  • Lymphoma, Mantle-Cell / enzymology
  • Lymphoma, Mantle-Cell / genetics
  • Lymphoma, Mantle-Cell / pathology
  • Male
  • Mice
  • Multiple Myeloma / drug therapy*
  • Multiple Myeloma / enzymology
  • Multiple Myeloma / genetics
  • Multiple Myeloma / pathology
  • Myeloid Cell Leukemia Sequence 1 Protein / genetics
  • Myeloid Cell Leukemia Sequence 1 Protein / metabolism
  • Pyridines / pharmacology*
  • Ubiquitin Thiolesterase / antagonists & inhibitors*
  • Ubiquitin Thiolesterase / genetics
  • Ubiquitin Thiolesterase / metabolism

Substances

  • Cyanoacrylates
  • Enzyme Inhibitors
  • MCL1 protein, human
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Pyridines
  • USP24 protein, human
  • USP9X protein, human
  • degrasyn
  • Ubiquitin Thiolesterase