Bone marrow fibroblasts overexpress miR-27b and miR-214 in step with multiple myeloma progression, dependent on tumour cell-derived exosomes

J Pathol. 2019 Feb;247(2):241-253. doi: 10.1002/path.5187.

Abstract

Aberrant microRNA (miR) expression has an important role in tumour progression, but its involvement in bone marrow fibroblasts of multiple myeloma patients remains undefined. We demonstrate that a specific miR profile in bone marrow fibroblasts parallels the transition from monoclonal gammopathy of undetermined significance (MGUS) to myeloma. Overexpression of miR-27b-3p and miR-214-3p triggers proliferation and apoptosis resistance in myeloma fibroblasts via the FBXW7 and PTEN/AKT/GSK3 pathways, respectively. Transient transfection of miR-27b-3p and miR-214-3p inhibitors demonstrates a cooperation between these two miRNAs in the expression of the anti-apoptotic factor MCL1, suggesting that miR-27b-3p and miR-214-3p negatively regulate myeloma fibroblast apoptosis. Furthermore, myeloma cells modulate miR-27b-3p and miR-214-3p expression in fibroblasts through the release of exosomes. Indeed, tumour cell-derived exosomes induce an overexpression of both miRNAs in MGUS fibroblasts not through a simple transfer mechanism but by de novo synthesis triggered by the transfer of exosomal WWC2 protein that regulates the Hippo pathway. Increased levels of miR-27b-3p and miR-214-3p in MGUS fibroblasts co-cultured with myeloma cell-derived exosomes enhance the expression of fibroblast activation markers αSMA and FAP. These data show that the MGUS-to-myeloma transition entails an aberrant miRNA profile in marrow fibroblasts and highlight a key role of myeloma cells in modifying the bone marrow microenvironment by reprogramming the marrow fibroblasts' behaviour. Copyright © 2018 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.

Keywords: MGUS; bone marrow fibroblasts; exosomes; miRNAs; multiple myeloma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Adult
  • Aged
  • Aged, 80 and over
  • Apoptosis
  • Bone Marrow Cells / metabolism*
  • Bone Marrow Cells / pathology
  • Cells, Cultured
  • Disease Progression
  • Endopeptidases
  • Exosomes / genetics
  • Exosomes / metabolism*
  • Exosomes / pathology
  • F-Box-WD Repeat-Containing Protein 7 / genetics
  • F-Box-WD Repeat-Containing Protein 7 / metabolism
  • Female
  • Fibroblasts / metabolism*
  • Fibroblasts / pathology
  • Gelatinases / metabolism
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Male
  • Membrane Proteins / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Middle Aged
  • Monoclonal Gammopathy of Undetermined Significance / genetics
  • Monoclonal Gammopathy of Undetermined Significance / metabolism*
  • Monoclonal Gammopathy of Undetermined Significance / pathology
  • Multiple Myeloma / genetics
  • Multiple Myeloma / metabolism*
  • Multiple Myeloma / pathology
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / metabolism
  • Serine Endopeptidases / metabolism
  • Signal Transduction
  • Tumor Microenvironment
  • Up-Regulation

Substances

  • ACTA2 protein, human
  • Actins
  • F-Box-WD Repeat-Containing Protein 7
  • FBXW7 protein, human
  • MIRN214 microRNA, human
  • MIRN27 microRNA, human
  • Membrane Proteins
  • MicroRNAs
  • PTEN Phosphohydrolase
  • PTEN protein, human
  • Endopeptidases
  • Serine Endopeptidases
  • fibroblast activation protein alpha
  • Gelatinases