miR-196b target screen reveals mechanisms maintaining leukemia stemness with therapeutic potential

J Exp Med. 2018 Aug 6;215(8):2115-2136. doi: 10.1084/jem.20171312. Epub 2018 Jul 11.

Abstract

We have shown that antagomiR inhibition of miRNA miR-21 and miR-196b activity is sufficient to ablate MLL-AF9 leukemia stem cells (LSC) in vivo. Here, we used an shRNA screening approach to mimic miRNA activity on experimentally verified miR-196b targets to identify functionally important and therapeutically relevant pathways downstream of oncogenic miRNA in MLL-r AML. We found Cdkn1b (p27Kip1) is a direct miR-196b target whose repression enhanced an embryonic stem cell-like signature associated with decreased leukemia latency and increased numbers of leukemia stem cells in vivo. Conversely, elevation of p27Kip1 significantly reduced MLL-r leukemia self-renewal, promoted monocytic differentiation of leukemic blasts, and induced cell death. Antagonism of miR-196b activity or pharmacologic inhibition of the Cks1-Skp2-containing SCF E3-ubiquitin ligase complex increased p27Kip1 and inhibited human AML growth. This work illustrates that understanding oncogenic miRNA target pathways can identify actionable targets in leukemia.

Publication types

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

MeSH terms

  • Animals
  • Carcinogenesis / genetics
  • Carcinogenesis / pathology
  • Cell Differentiation / genetics
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Cell Survival / genetics
  • Chromosomes, Human, Pair 11 / genetics
  • Cyclin-Dependent Kinase Inhibitor p27 / metabolism
  • Cyclin-Dependent Kinases / metabolism
  • Cyclins / metabolism
  • Embryonic Stem Cells / metabolism
  • Gene Expression Regulation, Leukemic
  • Humans
  • Leukemia, Myeloid, Acute / genetics
  • Leukemia, Myeloid, Acute / pathology*
  • Leukemia, Myeloid, Acute / therapy*
  • Mice, Inbred C57BL
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Neoplastic Stem Cells / metabolism*
  • Neoplastic Stem Cells / pathology*
  • Oncogenes
  • RNA, Small Interfering / metabolism

Substances

  • Cyclins
  • MIRN196 microRNA, human
  • MicroRNAs
  • RNA, Small Interfering
  • Cyclin-Dependent Kinase Inhibitor p27
  • Cyclin-Dependent Kinases