Mitochondrial Fission Mediates Endothelial Inflammation

Hypertension. 2020 Jul;76(1):267-276. doi: 10.1161/HYPERTENSIONAHA.120.14686. Epub 2020 May 11.

Abstract

Endothelial inflammation and mitochondrial dysfunction have been implicated in cardiovascular diseases, yet, a unifying mechanism tying them together remains limited. Mitochondrial dysfunction is frequently associated with mitochondrial fission/fragmentation mediated by the GTPase Drp1 (dynamin-related protein 1). Nuclear factor (NF)-κB, a master regulator of inflammation, is implicated in endothelial dysfunction and resultant complications. Here, we explore a causal relationship between mitochondrial fission and NF-κB activation in endothelial inflammatory responses. In cultured endothelial cells, TNF-α (tumor necrosis factor-α) or lipopolysaccharide induces mitochondrial fragmentation. Inhibition of Drp1 activity or expression suppresses mitochondrial fission, NF-κB activation, vascular cell adhesion molecule-1 induction, and leukocyte adhesion induced by these proinflammatory factors. Moreover, attenuations of inflammatory leukocyte adhesion were observed in Drp1 heterodeficient mice as well as endothelial Drp1 silenced mice. Intriguingly, inhibition of the canonical NF-κB signaling suppresses endothelial mitochondrial fission. Mechanistically, NF-κB p65/RelA seems to mediate inflammatory mitochondrial fission in endothelial cells. In addition, the classical anti-inflammatory drug, salicylate, seems to maintain mitochondrial fission/fusion balance against TNF-α via inhibition of NF-κB. In conclusion, our results suggest a previously unknown mechanism whereby the canonical NF-κB cascade and a mitochondrial fission pathway interdependently regulate endothelial inflammation.

Keywords: dynamins; endothelium; inflammation; leukocytes; mitochondria.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Animals
  • Aorta / cytology
  • Cell Adhesion
  • Cells, Cultured
  • Dynamins / antagonists & inhibitors
  • Dynamins / genetics
  • Dynamins / physiology*
  • Endothelial Cells / drug effects
  • Endothelial Cells / physiology*
  • Endothelium, Vascular / pathology*
  • Leukocytes, Mononuclear / cytology
  • Leukocytes, Mononuclear / metabolism
  • Membrane Proteins / physiology
  • Mice
  • Mitochondrial Dynamics / physiology*
  • Mitochondrial Proteins / physiology
  • Mutation, Missense
  • NF-kappa B / metabolism*
  • Phosphorylation
  • Phosphoserine / metabolism
  • Protein Processing, Post-Translational
  • Proteome
  • RNA Interference
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / pharmacology
  • Rats
  • Sodium Salicylate / pharmacology
  • Tumor Necrosis Factor-alpha / pharmacology
  • Vascular Cell Adhesion Molecule-1 / biosynthesis
  • Vascular Cell Adhesion Molecule-1 / genetics
  • Vasculitis / physiopathology*

Substances

  • Membrane Proteins
  • Mff protein, rat
  • Mitochondrial Proteins
  • NF-kappa B
  • Proteome
  • RNA, Small Interfering
  • Tumor Necrosis Factor-alpha
  • Vascular Cell Adhesion Molecule-1
  • Phosphoserine
  • Dnm1l protein, rat
  • Dynamins
  • Sodium Salicylate