Hypoxic tumor-derived exosomal miR-31-5p promotes lung adenocarcinoma metastasis by negatively regulating SATB2-reversed EMT and activating MEK/ERK signaling

J Exp Clin Cancer Res. 2021 Jun 1;40(1):179. doi: 10.1186/s13046-021-01979-7.

Abstract

Background: Exosomes have emerged as critical mediators of intercellular communication. Hypoxia is widely recognized as a key regulator of tumor aggressiveness, and significantly affects exosome release by tumor cells. However, the effects of exosomes derived from hypoxic lung adenocarcinoma (LUAD) cells are poorly understood.

Methods: Samples of miRNA isolated from hypoxic LUAD cell-derived exosomes (HExo) and normoxic LUAD cell-derived exosomes (NExo) were sequenced to identify miRNAs that might mediate tumor progression. Exosomal miRNA was co-cultured with LUAD cells to assess its biological effects on cell migration and metastasis both in vitro and in vivo. The cellular target of exosomal miRNA was confirmed by dual-luciferase assays. Western blot studies showed that exosomal miRNA regulated the related pathway. The availability of circulating exosomal miRNA derived from plasma was also evaluated.

Results: We found that HExo could significantly enhance the migration and invasion of normoxic LUAD cells. MiRNA sequencing results suggested that miR-31-5p was largely internalized within HExo and could be taken up by normoxic LUAD cells. Exosomal miR-31-5p was found to directly target Special AT-Rich Sequence-Binding Protein 2 (SATB2)-revered epithelial mesenchymal transition and significantly increase activation of MEK/ERK signaling, thereby contributing to tumor progression both in vitro and in vivo. Furthermore, higher levels of circulating exosomal miR-31-5p were detected in LUAD patients, especially in patients with metastatic disease.

Conclusions: Our findings demonstrate that exosomal miR-31-5p exerts a crucial role in LUAD progression, and could serve as a diagnostic biomarker for LUAD.

Keywords: Lung adenocarcinoma; SATB2; exosome; hypoxia; miR-31-5p.

MeSH terms

  • A549 Cells
  • Adenocarcinoma of Lung / genetics*
  • Adenocarcinoma of Lung / pathology
  • Animals
  • Cell Movement / genetics
  • Cell Proliferation / genetics*
  • Coculture Techniques
  • Epithelial-Mesenchymal Transition / genetics
  • Exosomes / genetics
  • Gene Expression Regulation, Neoplastic / genetics
  • Heterografts
  • Humans
  • MAP Kinase Signaling System / genetics
  • Matrix Attachment Region Binding Proteins / genetics*
  • Mice
  • MicroRNAs / genetics*
  • Neoplasm Invasiveness / genetics*
  • Neoplasm Invasiveness / pathology
  • Neoplasm Metastasis
  • Transcription Factors / genetics*
  • Tumor Hypoxia / genetics

Substances

  • MIRN31 microRNA, human
  • Matrix Attachment Region Binding Proteins
  • MicroRNAs
  • SATB2 protein, human
  • Transcription Factors