Nuclear-Cytoplasmic Transport Is a Therapeutic Target in Myelofibrosis

Clin Cancer Res. 2019 Apr 1;25(7):2323-2335. doi: 10.1158/1078-0432.CCR-18-0959. Epub 2018 Dec 18.

Abstract

Purpose: Myelofibrosis is a hematopoietic stem cell neoplasm characterized by bone marrow reticulin fibrosis, extramedullary hematopoiesis, and frequent transformation to acute myeloid leukemia. Constitutive activation of JAK/STAT signaling through mutations in JAK2, CALR, or MPL is central to myelofibrosis pathogenesis. JAK inhibitors such as ruxolitinib reduce symptoms and improve quality of life, but are not curative and do not prevent leukemic transformation, defining a need to identify better therapeutic targets in myelofibrosis.

Experimental design: A short hairpin RNA library screening was performed on JAK2V617F-mutant HEL cells. Nuclear-cytoplasmic transport (NCT) genes including RAN and RANBP2 were among top candidates. JAK2V617F-mutant cell lines, human primary myelofibrosis CD34+ cells, and a retroviral JAK2V617F-driven myeloproliferative neoplasms mouse model were used to determine the effects of inhibiting NCT with selective inhibitors of nuclear export compounds KPT-330 (selinexor) or KPT-8602 (eltanexor).

Results: JAK2V617F-mutant HEL, SET-2, and HEL cells resistant to JAK inhibition are exquisitely sensitive to RAN knockdown or pharmacologic inhibition by KPT-330 or KPT-8602. Inhibition of NCT selectively decreased viable cells and colony formation by myelofibrosis compared with cord blood CD34+ cells and enhanced ruxolitinib-mediated growth inhibition and apoptosis, both in newly diagnosed and ruxolitinib-exposed myelofibrosis cells. Inhibition of NCT in myelofibrosis CD34+ cells led to nuclear accumulation of p53. KPT-330 in combination with ruxolitinib-normalized white blood cells, hematocrit, spleen size, and architecture, and selectively reduced JAK2V617F-mutant cells in vivo.

Conclusions: Our data implicate NCT as a potential therapeutic target in myelofibrosis and provide a rationale for clinical evaluation in ruxolitinib-exposed patients with myelofibrosis.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects
  • Biological Transport / drug effects
  • Biomarkers
  • Cell Line, Tumor
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism*
  • Computational Biology / methods
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism*
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Gene Expression Profiling
  • Gene Knockdown Techniques
  • Humans
  • Janus Kinases / genetics
  • Janus Kinases / metabolism
  • Mice
  • Molecular Targeted Therapy
  • Mutation
  • Myeloproliferative Disorders / etiology
  • Myeloproliferative Disorders / metabolism
  • Myeloproliferative Disorders / pathology
  • Primary Myelofibrosis / drug therapy
  • Primary Myelofibrosis / etiology
  • Primary Myelofibrosis / metabolism*
  • STAT Transcription Factors / metabolism
  • Transcriptome

Substances

  • Antineoplastic Agents
  • Biomarkers
  • STAT Transcription Factors
  • Janus Kinases