Exploiting Protein Translation Dependence in Multiple Myeloma with Omacetaxine-Based Therapy

Clin Cancer Res. 2021 Feb 1;27(3):819-830. doi: 10.1158/1078-0432.CCR-20-2246. Epub 2020 Oct 27.

Abstract

Purpose: The prognosis of patients with multiple myeloma who are resistant to proteasome inhibitors, immunomodulatory drugs (IMiD), and daratumumab is extremely poor. Even B-cell maturation antigen-specific chimeric antigen receptor T-cell therapies provide only a temporary benefit before patients succumb to their disease. In this article, we interrogate the unique sensitivity of multiple myeloma cells to the alternative strategy of blocking protein translation with omacetaxine.

Experimental design: We determined protein translation levels (n = 17) and sensitivity to omacetaxine (n = 51) of primary multiple myeloma patient samples. Synergy was evaluated between omacetaxine and IMiDs in vitro, ex vivo, and in vivo. Underlying mechanism was investigated via proteomic analysis.

Results: Almost universally, primary patient multiple myeloma cells exhibit >2.5-fold increased rates of protein translation compared with normal marrow cells. Ex vivo treatment with omacetaxine resulted in >50% reduction in viable multiple myeloma cells. In this cohort, high levels of translation serve as a biomarker for patient multiple myeloma cell sensitivity to omacetaxine. Unexpectedly, omacetaxine demonstrated synergy with IMiDs in multiple myeloma cell lines in vitro. In addition, in an IMiD-resistant relapsed patient sample, omacetaxine/IMiD combination treatment resensitized the multiple myeloma cells to the IMiD. Proteomic analysis found that the omacetaxine/IMiD combination treatment produced a double-hit on the IRF4/c-MYC pathway, which is critical to multiple myeloma survival.

Conclusions: Overall, protein translation inhibitors represent a potential new drug class for myeloma treatment and provide a rationale for conducting clinical trials with omacetaxine alone and in combination with IMiDs for patients with relapsed/refractory multiple myeloma.

Publication types

  • Observational Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Bone Marrow / pathology
  • Drug Resistance, Neoplasm / drug effects
  • Drug Screening Assays, Antitumor
  • Drug Synergism
  • Homoharringtonine / pharmacology*
  • Homoharringtonine / therapeutic use
  • Humans
  • Immunomodulating Agents / pharmacology
  • Immunomodulating Agents / therapeutic use
  • Interferon Regulatory Factors / antagonists & inhibitors
  • Interferon Regulatory Factors / metabolism
  • Mice
  • Multiple Myeloma / drug therapy*
  • Multiple Myeloma / pathology
  • Primary Cell Culture
  • Protein Biosynthesis / drug effects*
  • Protein Synthesis Inhibitors / pharmacology*
  • Protein Synthesis Inhibitors / therapeutic use
  • Proto-Oncogene Proteins c-myc / antagonists & inhibitors
  • Proto-Oncogene Proteins c-myc / metabolism
  • Signal Transduction / drug effects
  • Tumor Cells, Cultured
  • Xenograft Model Antitumor Assays

Substances

  • Immunomodulating Agents
  • Interferon Regulatory Factors
  • MYC protein, human
  • Protein Synthesis Inhibitors
  • Proto-Oncogene Proteins c-myc
  • interferon regulatory factor-4
  • Homoharringtonine