Partial Inhibition of Glycolysis Reduces Atherogenesis Independent of Intraplaque Neovascularization in Mice

Arterioscler Thromb Vasc Biol. 2020 May;40(5):1168-1181. doi: 10.1161/ATVBAHA.119.313692. Epub 2020 Mar 19.

Abstract

Objective: Intraplaque neovascularization is an important feature of unstable human atherosclerotic plaques. However, its impact on plaque formation and stability is poorly studied. Because proliferating endothelial cells generate up to 85% of their ATP from glycolysis, we investigated whether pharmacological inhibition of glycolytic flux by the small-molecule 3PO (3-[3-pyridinyl]-1-[4-pyridinyl]-2-propen-1-one) could have beneficial effects on plaque formation and composition. Approach and Results: ApoE-/- (apolipoprotein E deficient) mice treated with 3PO (50 µg/g, ip; 4×/wk, 4 weeks) showed a metabolic switch toward ketone body formation. Treatment of ApoE-/-Fbn1C1039G+/- mice with 3PO (50 µg/g, ip) either after 4 (preventive, twice/wk, 10 weeks) or 16 weeks of Western diet (curative, 4×/wk, 4 weeks) inhibited intraplaque neovascularization by 50% and 38%, respectively. Plaque formation was significantly reduced in all 3PO-treated animals. This effect was independent of intraplaque neovascularization. In vitro experiments showed that 3PO favors an anti-inflammatory M2 macrophage subtype and suppresses an M1 proinflammatory phenotype. Moreover, 3PO induced autophagy, which in turn impaired NF-κB (nuclear factor-kappa B) signaling and inhibited TNF-α (tumor necrosis factor-alpha)-mediated VCAM-1 (vascular cell adhesion molecule-1) and ICAM-1 (intercellular adhesion molecule-1) upregulation. Consistently, a preventive 3PO regimen reduced endothelial VCAM-1 expression in vivo. Furthermore, 3PO improved cardiac function in ApoE-/-Fbn1C1039G+/- mice after 10 weeks of treatment.

Conclusions: Partial inhibition of glycolysis restrained intraplaque angiogenesis without affecting plaque composition. However, less plaques were formed, which was accompanied by downregulation of endothelial adhesion molecules-an event that depends on autophagy induction. Inhibition of coronary plaque formation by 3PO resulted in an overall improved cardiac function.

Keywords: animals; atherosclerosis; autophagy; glycolysis; mice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arteries / drug effects*
  • Arteries / metabolism
  • Arteries / pathology
  • Atherosclerosis / drug therapy*
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • Autophagy / drug effects
  • Cells, Cultured
  • Disease Models, Animal
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Female
  • Fibrillin-1 / genetics
  • Fibrillin-1 / metabolism
  • Glycolysis / drug effects*
  • Humans
  • Intercellular Adhesion Molecule-1 / metabolism
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / pathology
  • Mice, Knockout, ApoE
  • NF-kappa B / metabolism
  • Neovascularization, Pathologic*
  • Phenotype
  • Plaque, Atherosclerotic*
  • Pyridines / pharmacology*
  • Vascular Cell Adhesion Molecule-1 / metabolism

Substances

  • 3-(3-pyridinyl)-1-(4-pyridinyl)-2-propen-1-one
  • Fbn1 protein, mouse
  • Fibrillin-1
  • ICAM1 protein, human
  • NF-kappa B
  • Pyridines
  • Vascular Cell Adhesion Molecule-1
  • Intercellular Adhesion Molecule-1