miR-221/222 suppression induced by activation of the cAMP/PKA/CREB1 pathway is required for cAMP-induced bidirectional differentiation of glioma cells

FEBS Lett. 2021 Nov;595(22):2829-2843. doi: 10.1002/1873-3468.14208. Epub 2021 Oct 27.

Abstract

Factors that increase cAMP levels can induce lineage-specific differentiation of glioma cells into astrocyte-like cells. However, the differentiation pattern and underlying mechanisms remain unclear. Here, we find that cAMP/protein kinase A (PKA)/cAMP responsive element binding protein 1 (CREB1)-induced miR-221/222 suppression contributes to the neuron-like differentiation of gliomas. cAMP agonists selectively induced neuron- and astrocyte-like but not oligodendrocyte-like differentiation of C6 glioma cells. PKA inhibitors and CREB1 knockout blocked neuron-like differentiation of glioma cells. cAMP inhibited miR-221/222 in a PKA/CREB1-dependent manner. Importantly, both in vitro and in vivo assays demonstrated that transcriptional suppression of miR-221/222 is required for neuronal differentiation of glioma cells. Our findings suggest that increasing cAMP levels can induce bidirectional differentiation of glioma cells. Furthermore, the miR-221/222 cluster acts as an epigenetic brake during glioma differentiation.

Keywords: cAMP responsive element binding protein 1; cyclic adenosine monophosphate; differentiation; glioma; microRNA; protein kinase A.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / cytology
  • Astrocytes / metabolism
  • Brain Neoplasms / metabolism*
  • Brain Neoplasms / pathology
  • Cell Differentiation*
  • Cell Line, Tumor
  • Cell Lineage
  • Cyclic AMP / metabolism*
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Female
  • Glioma / metabolism*
  • Glioma / pathology
  • HEK293 Cells
  • Humans
  • Mice
  • Mice, Inbred BALB C
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Neurons / cytology
  • Neurons / metabolism
  • Rats

Substances

  • Creb1 protein, rat
  • Cyclic AMP Response Element-Binding Protein
  • MIRN221 microRNA, rat
  • MIRN222 microRNA, rat
  • MicroRNAs
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases