MFN2-dependent mitochondrial dysfunction contributes to Relm-β-induced pulmonary arterial hypertension via USP18/Twist1/miR-214 pathway

Eur J Pharmacol. 2024 Oct 5:980:176828. doi: 10.1016/j.ejphar.2024.176828. Epub 2024 Jul 31.

Abstract

Induction of resistin-like molecule β (Relm-β) and mitofusin 2 (MFN2) mediated aberrant mitochondrial fission have been found to be involved in the pathogenesis of pulmonary arterial hypertension (PAH). However, the molecular mechanisms underlying Relm-β regulation of MFN2 therefore mitochondrial fission remain unclear. This study aims to address these issues. Primary cultured PASMCs and monocrotaline (MCT)-induced PAH rats were applied in this study. The results showed that Relm-β promoted cells proliferation in PASMCs, this was accompanied with the upregulation of USP18, Twist1 and miR-214, and downregulation of MFN2. We found that Relm-β increased USP18 expression which in turn raised Twist1 by suppressing its proteasome degradation. Elevation of Twist1 increased miR-214 expression and then reduced MFN2 expression and mitochondrial fragmentation leading to PASMCs proliferation. In vivo study, we confirmed that Relm-β was elevated in MCT-induced PAH rat model, and USP18/Twist1/miR-214/MFN2 axis was altered similar as in vitro. Targeting this cascade by Relm-β receptor inhibitor Calhex231, proteasome inhibitor MG-132, Twist1 inhibitor Harmine or miR-214 antagomiR prevented the development of pulmonary vascular remodeling and therefore PAH in MCT-treated rats. In conclusion, we demonstrate that Relm-β promotes PASMCs proliferation and vascular remodeling by activating USP18/Twist1/miR-214 dependent MFN2 reduction and mitochondrial fission, suggesting that this signaling pathway might be a promising target for management of PAH.

Keywords: MFN2; Pulmonary arterial hypertension; Relm-β; Twist1; USP18.

MeSH terms

  • Animals
  • Cell Proliferation* / drug effects
  • GTP Phosphohydrolases* / metabolism
  • Hypertension, Pulmonary / chemically induced
  • Hypertension, Pulmonary / metabolism
  • Hypertension, Pulmonary / pathology
  • Hypertension, Pulmonary / physiopathology
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Male
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Mitochondria* / drug effects
  • Mitochondria* / metabolism
  • Mitochondrial Dynamics / drug effects
  • Mitochondrial Proteins
  • Monocrotaline / toxicity
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism
  • Myocytes, Smooth Muscle / pathology
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Pulmonary Arterial Hypertension / chemically induced
  • Pulmonary Arterial Hypertension / metabolism
  • Pulmonary Arterial Hypertension / pathology
  • Pulmonary Arterial Hypertension / physiopathology
  • Pulmonary Artery / drug effects
  • Pulmonary Artery / metabolism
  • Pulmonary Artery / pathology
  • Rats
  • Rats, Sprague-Dawley*
  • Signal Transduction* / drug effects
  • Twist-Related Protein 1* / genetics
  • Twist-Related Protein 1* / metabolism
  • Ubiquitin Thiolesterase* / genetics
  • Ubiquitin Thiolesterase* / metabolism

Substances

  • GTP Phosphohydrolases
  • Intercellular Signaling Peptides and Proteins
  • Mfn2 protein, rat
  • MicroRNAs
  • Mirn214 microRNA, rat
  • Mitochondrial Proteins
  • Monocrotaline
  • Nuclear Proteins
  • Twist-Related Protein 1
  • Ubiquitin Thiolesterase
  • Usp18 protein, rat
  • Twist1 protein, rat