Multiple myeloma-derived exosomes are enriched of amphiregulin (AREG) and activate the epidermal growth factor pathway in the bone microenvironment leading to osteoclastogenesis

J Hematol Oncol. 2019 Jan 8;12(1):2. doi: 10.1186/s13045-018-0689-y.

Abstract

Background: Multiple myeloma (MM) is a clonal plasma cell malignancy associated with osteolytic bone disease. Recently, the role of MM-derived exosomes in the osteoclastogenesis has been demonstrated although the underlying mechanism is still unknown. Since exosomes-derived epidermal growth factor receptor ligands (EGFR) are involved in tumor-associated osteolysis, we hypothesize that the EGFR ligand amphiregulin (AREG) can be delivered by MM-derived exosomes and participate in MM-induced osteoclastogenesis.

Methods: Exosomes were isolated from the conditioned medium of MM1.S cell line and from bone marrow (BM) plasma samples of MM patients. The murine cell line RAW264.7 and primary human CD14+ cells were used as osteoclast (OC) sources.

Results: We found that AREG was specifically enriched in exosomes from MM samples and that exosomes-derived AREG led to the activation of EGFR in pre-OC, as showed by the increase of mRNA expression of its downstream SNAIL in both RAW264.7 and CD14+ cells. The presence of neutralizing anti-AREG monoclonal antibody (mAb) reverted this effect. Consequently, we showed that the effect of MM-derived exosomes on osteoclast differentiation was inhibited by the pre-treatment of exosomes with anti-AREG mAb. In addition, we demonstrated the ability of MM-derived AREG-enriched exosomes to be internalized into human mesenchymal stromal cells (MSCs) blocking osteoblast (OB) differentiation, increasing MM cell adhesion and the release of the pro-osteoclastogenic cytokine interleukin-8 (IL8). Accordingly, anti-AREG mAb inhibited the release of IL8 by MSCs suggesting that both direct and indirect effects are responsible for AREG-enriched exosomes involvement on MM-induced osteoclastogenesis.

Conclusions: In conclusion, our data indicate that AREG is packed into MM-derived exosomes and implicated in OC differentiation through an indirect mechanism mediated by OBs.

Keywords: Amphiregulin; Bone disease; Epidermal growth factor receptor; Exosomes; Interleukin 8; Multiple myeloma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amphiregulin / genetics*
  • Amphiregulin / immunology
  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Cell Adhesion
  • Cell Differentiation
  • Cell Line, Tumor
  • Epidermal Growth Factor / metabolism*
  • ErbB Receptors / genetics
  • ErbB Receptors / metabolism
  • Exosomes / metabolism*
  • Humans
  • Interleukin-8 / antagonists & inhibitors
  • Ligands
  • Mesenchymal Stem Cells
  • Mice
  • Multiple Myeloma / metabolism*
  • Multiple Myeloma / pathology
  • Osteoblasts / metabolism
  • Osteoclasts / metabolism
  • Osteogenesis*
  • RAW 264.7 Cells
  • Tumor Microenvironment*

Substances

  • AREG protein, human
  • Amphiregulin
  • Antibodies, Monoclonal
  • CXCL8 protein, human
  • Interleukin-8
  • Ligands
  • Epidermal Growth Factor
  • EGFR protein, human
  • ErbB Receptors