Cross-talk between oxidized LDL, oxidative stress and renin-angiotensin-aldosterone system

https://doi.org/10.1007/s00392-025-02625-4

Henning Morawietz (Dresden)1, R. Catar (Berlin)2, J. Kamhieh-Milz (Berlin)3, C. Goettsch (Aachen)4, L. Chen (Berlin)2, D. Zickler (Berlin)2, A. Taye (1464040)5, A. Hofmann (01307)6, C. Brunßen (Dresden)1, G. Müller (Dresden)1, M. Cybularz-Bednarek (Dresden)7, C. Hengst (Dresden)1, M. D. L. Villar Ballesteros (Dresden)1, S. Lehmann (Dresden)8, U. Schubert (Dresden)8, B. Ludwig (Dresden)8, C. Zeigler (Dresden)8, S. Bornstein (Dresden)8, A. Krug (Dresden)8, T. Walther (Berlin)9, G. Moll (Berlin)2

1Universitätsklinikum Carl Gustav Carus an der TU Dresden Med. Klinik III, Gefäßendothel/Mikrozirkulation Dresden, Deutschland; 2Charité - Universitätsmedizin Berlin Berlin, Deutschland; 3Charité Universitätsmedizin Berlin Institute of Transfusion Medicine Berlin, Deutschland; 4Uniklinik RWTH Aachen Med. Klinik I - Kardiologie, Angiologie und Internistische Intensivmedizin Aachen, Deutschland; 5South Valley University Department of Pharmacology and Toxicology, Faculty of Pharmacy 1464040, Ägypten; 6University Hospital Carl Gustav Carus, TU Dresden Division of Vascular and Endovascular Surgery, Department of Visceral, Thoracic and Vascular Surgery 01307, Deutschland; 7Herzzentrum Dresden GmbH an der TU Dresden Klinik für Innere Medizin, Kardiologie und Intensivmedizin Dresden, Deutschland; 8Universitätsklinikum Carl Gustav Carus, TU Dresden Med. Klinik III Dresden, Deutschland; 9Medical School Berlin (MSB) Berlin, Deutschland

 

Background: Hypertension and hypercholesterolemia are important risk factors of endothelial dysfunction and atherosclerosis. Previous studies suggested a crosstalk between an activated renin-angiotensin-aldosterone system (RAAS), reactive oxygen species (ROS) and oxidized low-density lipoproteins (oxLDL) in atherosclerosis, but the underlying molecular mechanisms are not well understood.

Hypothesis: Can we identify novel signaling pathways controlling the molecular crosstalk of the RAAS with ROS and oxLDL in endothelial dysfunction and atherosclerosis?

Methods: The impact of AT1R blockade on oxLDL-induced superoxide anion formation and endothelial dysfunction was studied in human umbilical artery endothelial cells and aortic rings of wild-type mice by chemiluminescence and Mulvany myograph. We cloned 5’-terminal deletions of the AT1R promoter and assessed the luciferase activity in human endothelial cells. Oct-1 binding to the human AT1R promoter region was studied by EMSA. Further assays included real-time PCR, confocal microscopy, Western blotting, G protein reporter assays, phospho-ERK1/2 antibodies and specific siRNAs. The data were validated in heart of obese C57BL/6 mice and cardiac and aortic tissue of AT1a/AT1b double knockout mice in vivo.

Results: AT1R promoter activation studies upon Ang II- and oxLDL-stimulation in endothelial cells revealed that Ang II and oxLDL activate AT1R signaling through G protein Gα12/13, followed by activation of ERK1/2 MAP kinases, and transcription and translation of Oct-1, resulting in up-regulation of AT1R, LOX-1 and NOX2 expression, which could be antagonized by specific inhibitors at each step of the identified signaling cascade. AT1R blockade improved oxLDL-induced endothelial dysfunction in aortic rings of wild-type mice. Male C57BL/6 mice fed a high-fat diet exhibited upregulation of Oct-1 levels in cardiac tissues, compared to normal controls, while AT1a/AT1b double knockout mice demonstrated downregulation of Oct-1, AT1R, LOX-1, and NOX2 on mRNA and protein level in cardiac and aorta tissue, thus confirming the identified signaling cascade in vivo.

Conclusions: Oct-1 is an essential transcription factor for Ang II- and oxLDL-induced upregulation of AT1R and LOX-1 expression in endothelium, thus identifying a novel molecular cross-talk of oxLDL with ROS signaling and the RAAS contributing to development of endothelial dysfunction and atherosclerosis.

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