Innate Immune System Regulated by Stimulator of Interferon Genes, a Cytosolic DNA Sensor, Regulates Endothelial Function

J Am Heart Assoc. 2023 Nov 21;12(22):e030084. doi: 10.1161/JAHA.123.030084. Epub 2023 Nov 10.

Abstract

Background: Sterile inflammation caused by metabolic disorders impairs endothelial function; however, the underlying mechanism by which hyperglycemia induces inflammation remains obscure. Recent studies have suggested that stimulator of interferon genes (STING), a key cytosolic DNA sensor in the innate immune system, contributes to the pathogenesis of inflammatory diseases. This study examines the role of the STING in endothelial dysfunction in streptozotocin-induced diabetic mice.

Methods and results: Injection of streptozotocin promoted the expression of STING and DNA damage markers in the aorta of wild-type mice. Streptozotocin elevated blood glucose and lipid levels in both wild-type and STING-deficient mice, which showed no statistical differences. Genetic deletion of STING ameliorated endothelial dysfunction as determined by the vascular relaxation in response to acetylcholine (P<0.001) and increased endothelial nitric oxide synthase phosphorylation in the aorta (P<0.05) in STZ-injected mice. Endothelium-independent vascular response to sodium nitroprusside did not differ. Treatment with a direct STING agonist, cyclic GMP-AMP, or mitochondrial DNA increased inflammatory molecule expression (eg, VCAM1 and IFNB) and decreased endothelial nitric oxide synthase phosphorylation in human umbilical vein endothelial cells, partially through the STING pathway. Cyclic GMP-AMP significantly impaired endothelial function of aortic segments obtained from wild-type mice, which was ameliorated in the presence of C-176, a STING inhibitor, or a neutralizing interferon-β antibody. Furthermore, the administration of C-176 ameliorated endothelial dysfunction in STZ-induced diabetic mice (P<0.01).

Conclusions: The DNA damage response regulated by STING impairs endothelial function. STING signaling may be a potential therapeutic target of endothelial dysfunction caused by hyperglycemia.

Keywords: STING; diabetes; endothelial function; inflammation.

MeSH terms

  • Animals
  • DNA Damage
  • DNA, Mitochondrial / genetics
  • DNA, Mitochondrial / metabolism
  • Diabetes Mellitus, Experimental* / metabolism
  • Diabetes Mellitus, Experimental* / physiopathology
  • Endothelium, Vascular* / drug effects
  • Endothelium, Vascular* / metabolism
  • Endothelium, Vascular* / physiopathology
  • Human Umbilical Vein Endothelial Cells* / drug effects
  • Human Umbilical Vein Endothelial Cells* / metabolism
  • Humans
  • Immunity, Innate*
  • Male
  • Membrane Proteins* / genetics
  • Membrane Proteins* / metabolism
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Knockout
  • Nitric Oxide Synthase Type III* / metabolism
  • Nucleotides, Cyclic / metabolism
  • Nucleotides, Cyclic / pharmacology
  • Phosphorylation
  • Signal Transduction
  • Vasodilation / drug effects

Substances

  • Sting1 protein, mouse
  • Membrane Proteins
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • cyclic guanosine monophosphate-adenosine monophosphate
  • STING1 protein, human
  • DNA, Mitochondrial
  • Nucleotides, Cyclic
  • NOS3 protein, human