Endothelial LOX-1 activation differentially regulates arterial thrombus formation depending on oxLDL levels: role of the Oct-1/SIRT1 and ERK1/2 pathways

Cardiovasc Res. 2017 Apr 1;113(5):498-507. doi: 10.1093/cvr/cvx015.

Abstract

Aims: The lectin-like oxLDL receptor-1 (LOX-1) promotes endothelial uptake of oxidized low-density lipoprotein (oxLDL) and plays an important role in atherosclerosis and acute coronary syndromes (ACS). However, its role in arterial thrombus formation remains unknown. We investigated whether LOX-1 plays a role in arterial thrombus formation in vivo at different levels of oxLDL using endothelial-specific LOX-1 transgenic mice (LOX-1TG) and a photochemical injury thrombosis model of the carotid artery.

Methods and results: In mice fed a normal chow diet, time to arterial occlusion was unexpectedly prolonged in LOX-1TG as compared to WT. In line with this, tissue factor (TF) expression and activity in carotid arteries of LOX-1TG mice were reduced by half. This effect was mediated by activation of octamer transcription factor 1 (Oct-1) leading to upregulation of the mammalian deacetylase silent information regulator-two 1 (SIRT1) via binding to its promoter and subsequent inhibition of NF-κB signaling. In contrast, intravenous injection of oxLDL as well as high cholesterol diet for 6 weeks led to a switch from the Oct-1/SIRT1 signal transduction pathway to the ERK1/2 pathway and in turn to an enhanced thrombotic response with shortened occlusion time.

Conclusions: Thus, LOX-1 differentially regulates thrombus formation in vivo depending on the degree of activation by oxLDL. At low oxLDL levels LOX-1 activates the protective Oct-1/SIRT1 pathway, while at higher levels of the lipoprotein switches to the thrombogenic ERK1/2 pathway. These findings may be important for arterial thrombus formation in ACS and suggest that SIRT1 may represent a novel therapeutic target in this context.

Keywords: LOX-1 • Arterial thrombosis • Endothelium • Tissue factor.

MeSH terms

  • Animals
  • Binding Sites
  • Blood Coagulation*
  • Carotid Arteries / enzymology*
  • Carotid Artery Injuries / blood
  • Carotid Artery Injuries / enzymology*
  • Carotid Artery Injuries / genetics
  • Cholesterol, Dietary
  • Disease Models, Animal
  • Genetic Predisposition to Disease
  • Humans
  • Lipoproteins, LDL / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mitogen-Activated Protein Kinase 1 / metabolism*
  • Mitogen-Activated Protein Kinase 3 / metabolism*
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Octamer Transcription Factor-1 / genetics
  • Octamer Transcription Factor-1 / metabolism*
  • Phenotype
  • Phosphorylation
  • Promoter Regions, Genetic
  • Scavenger Receptors, Class E / genetics
  • Scavenger Receptors, Class E / metabolism*
  • Signal Transduction
  • Sirtuin 1 / genetics
  • Sirtuin 1 / metabolism*
  • Thromboplastin / metabolism
  • Thrombosis / blood
  • Thrombosis / enzymology*
  • Thrombosis / genetics
  • Thrombosis / prevention & control
  • Time Factors

Substances

  • Cholesterol, Dietary
  • Lipoproteins, LDL
  • NF-kappa B
  • Octamer Transcription Factor-1
  • Olr1 protein, mouse
  • Pou2f1 protein, mouse
  • Scavenger Receptors, Class E
  • oxidized low density lipoprotein
  • Thromboplastin
  • Mapk1 protein, mouse
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Sirt1 protein, mouse
  • Sirtuin 1