Role of the CCL5 and Its Receptor, CCR5, in the Genesis of Aldosterone-Induced Hypertension, Vascular Dysfunction, and End-Organ Damage

Hypertension. 2024 Apr;81(4):776-786. doi: 10.1161/HYPERTENSIONAHA.123.21888. Epub 2024 Jan 19.

Abstract

Background: Aldosterone has been described to initiate cardiovascular diseases by triggering exacerbated sterile vascular inflammation. The functions of CCL5 (C-C motif chemokine ligand 5) and its receptor CCR5 (C-C motif chemokine receptor 5) are well known in infectious diseases, their contributions to aldosterone-induced vascular injury and hypertension remain unknown.

Methods: We analyzed the vascular profile, blood pressure, and renal damage in wild-type (CCR5+/+) and CCR5 knockout (CCR5-/-) mice treated with aldosterone (600 µg/kg per day for 14 days) while receiving 1% saline to drink. Vascular function was analyzed in aorta and mesenteric arteries, blood pressure was measured by telemetry and renal injury and inflammation were analyzed via histology and flow cytometry. Endothelial cells were used to study the molecular signaling whereby CCL5 induces endothelial dysfunction.

Results: Aldosterone treatment resulted in exaggerated CCL5 circulating levels and vascular CCR5 expression in CCR5+/+ mice accompanied by endothelial dysfunction, hypertension, and renal inflammation and damage. CCR5-/- mice were protected from these aldosterone-induced effects. Mechanistically, we demonstrated that CCL5 increased NOX1 (NADPH oxidase 1) expression, reactive oxygen species formation, NFκB (nuclear factor kappa B) activation, and inflammation and reduced NO production in isolated endothelial cells. These effects were abolished by antagonizing CCR5 with Maraviroc. Finally, aorta incubated with CCL5 displayed severe endothelial dysfunction, which is prevented by blocking NOX1, NFκB, or CCR5.

Conclusions: Our data demonstrate that CCL5/CCR5, through activation of NFκB and NOX1, is critically involved in aldosterone-induced vascular and renal damage and hypertension placing CCL5 and CCR5 as potential therapeutic targets for conditions characterized by aldosterone excess.

Keywords: NADPH oxidases; aldosterone; chemokines; chemokines receptors; oxidative stress.

MeSH terms

  • Aldosterone* / pharmacology
  • Animals
  • Chemokine CCL5* / genetics
  • Chemokine CCL5* / metabolism
  • Endothelial Cells / metabolism
  • Hypertension* / chemically induced
  • Hypertension* / metabolism
  • Inflammation
  • Mice
  • Receptors, CCR5* / genetics
  • Receptors, CCR5* / metabolism

Substances

  • Aldosterone
  • Receptors, CCR5
  • CCR5 protein, mouse
  • Ccl5 protein, mouse
  • Chemokine CCL5