MicroRNA-211 Modulates the DUSP6-ERK5 Signaling Axis to Promote BRAFV600E-Driven Melanoma Growth In Vivo and BRAF/MEK Inhibitor Resistance

J Invest Dermatol. 2021 Feb;141(2):385-394. doi: 10.1016/j.jid.2020.06.038. Epub 2020 Sep 2.

Abstract

MicroRNAs (miRs) are important posttranscriptional regulators of cell fate in both normal and disease states. miR-211 has previously been shown to be a direct regulator of metabolism in BRAFV600E-mutant melanoma cells in vitro. Here, we report that miR-211 expression promotes the aggressive growth of BRAFV600E-mutant melanoma xenografts in vivo. miR-211 promoted proliferation through the posttranscriptional activation of extracellular signal-regulated kinase (ERK) 5 signaling, which has recently been implicated in the resistance to BRAF and MAPK/ERK kinase inhibitors. We therefore examined whether miR-211 similarly modulated melanoma resistance to the BRAF inhibitor vemurafenib and the MAPK/ERK kinase inhibitor cobimetinib. Consistent with this model, miR-211 expression increased melanoma cell resistance to both the inhibitors, and this resistance was associated with an increased ERK5 phosphorylation. miR-211 mediates these effects by directly inhibiting the expression of DUSP6, an ERK5 pathway-specific phosphatase and now shown to be an miR-211 target gene. These results dissect the role of the miR-211-DUSP6-ERK5 axis in melanoma tumor growth and suggest a mechanism for the development of drug-resistant tumors and a target for overcoming resistance.

Publication types

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

MeSH terms

  • Animals
  • Azetidines / pharmacology
  • Azetidines / therapeutic use
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Drug Resistance, Neoplasm / genetics*
  • Dual Specificity Phosphatase 6 / genetics*
  • Dual Specificity Phosphatase 6 / metabolism
  • Gene Knockdown Techniques
  • Humans
  • MAP Kinase Signaling System / genetics
  • Melanoma / drug therapy*
  • Melanoma / genetics
  • Melanoma / pathology
  • Mice
  • MicroRNAs / metabolism*
  • Mitogen-Activated Protein Kinase 7 / genetics
  • Mitogen-Activated Protein Kinase 7 / metabolism*
  • Mutation
  • Phosphorylation / genetics
  • Piperidines / pharmacology
  • Piperidines / therapeutic use
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Kinase Inhibitors / therapeutic use
  • Proto-Oncogene Proteins B-raf / antagonists & inhibitors
  • Proto-Oncogene Proteins B-raf / genetics
  • Proto-Oncogene Proteins B-raf / metabolism
  • Vemurafenib / pharmacology
  • Vemurafenib / therapeutic use
  • Xenograft Model Antitumor Assays

Substances

  • Azetidines
  • MIRN211 microRNA, human
  • MicroRNAs
  • Piperidines
  • Protein Kinase Inhibitors
  • Vemurafenib
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf
  • MAPK7 protein, human
  • Mitogen-Activated Protein Kinase 7
  • DUSP6 protein, human
  • Dual Specificity Phosphatase 6
  • cobimetinib