Hyperbaric oxygen boosts long noncoding RNA MALAT1 exosome secretion to suppress microRNA-92a expression in therapeutic angiogenesis

Int J Cardiol. 2019 Jan 1:274:271-278. doi: 10.1016/j.ijcard.2018.09.118. Epub 2018 Oct 2.

Abstract

Background: Hyperbaric oxygen (HBO) could improve wound healing by enhancement of angiogenesis. The effect of HBO on metastasis-associated lung adenocarcinoma transcript 1 (MALAT1), a proangiogenic long noncoding RNA, and on endothelial cell-derived exosome is unknown. We aim to investigate both whether MALAT1 is altered in human coronary artery endothelial cells (HCAECs)-derived exosomes in response to HBO as well as the molecular regulatory mechanisms of MALAT1 in HCAECs under HBO treatment.

Methods and results: HCAECs were cultured and HBO was applied at 2.5 atmosphere absolute (ATA) in a hyperbaric chamber. Exosomes were extracted from culture media. A rat model of hind-limb ischemia was performed by ligation of the right femoral artery. HBO at 2.5 ATA significantly increased MALAT1 expression in HCAECs and HCAECs-derived exosomes. MALAT1 suppressed miR-92a expression in HCAEC-derived exosomes under HBO. Silencing MALAT1 by MALAT1 siRNA significantly inhibited KLF2 mRNA expression induced by HBO, as did MiR-92a. MiR-92a significantly decreased KLF2 luciferase activity in HCAECs under HBO. HBO and HBO-induced exosomes significantly increased cell proliferation and the capillary-like network formation of HCAECs. MALAT1 siRNA and miR-92a overexpression significantly attenuated the cell proliferation and tube formation caused by HBO-induced exosome. HBO and HBO-induced exosomes significantly improved neovascularization in a rat model of hind-limb ischemia.

Conclusions: HBO upregulates MALAT1 to suppress miR-92a expression and counteracts the inhibitory effect of miR-92a on KLF2 expression in HCAECs to enhance neovascularization. HBO-induced derivation of exosomes from HCAECs enhances angiogenesis. Exosomes containing MALAT1 might serve as a valuable therapeutic tool for neovascularization by HBO.

Keywords: Coronary artery endothelial cells; Exosome; Hyperbaric oxygen; MALAT1; microRNA-92a.

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Proliferation
  • Cells, Cultured
  • Coronary Vessels / metabolism*
  • Coronary Vessels / pathology
  • Disease Models, Animal
  • Endothelium, Vascular / metabolism*
  • Endothelium, Vascular / pathology
  • Exosomes / metabolism
  • Humans
  • Hyperbaric Oxygenation / methods*
  • Male
  • MicroRNAs / biosynthesis
  • MicroRNAs / genetics*
  • Myocardial Ischemia / genetics*
  • Myocardial Ischemia / pathology
  • Myocardial Ischemia / therapy
  • Neovascularization, Physiologic / genetics
  • RNA / genetics
  • RNA, Long Noncoding / genetics*
  • RNA, Long Noncoding / metabolism
  • Rats
  • Rats, Wistar
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • MALAT1 long noncoding RNA, rat
  • MIRN92 microRNA, human
  • MicroRNAs
  • RNA, Long Noncoding
  • RNA