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A RGS7-CaMKII complex drives myocyte-intrinsic and myocyte-extrinsic mechanisms of chemotherapy-induced cardiotoxicity
Journal article   Open access   Peer reviewed

A RGS7-CaMKII complex drives myocyte-intrinsic and myocyte-extrinsic mechanisms of chemotherapy-induced cardiotoxicity

Madhuri Basak, Abhishek Singh Sengar, Kiran Das, Tarun Mahata, Manish Kumar, Dinesh Kumar, Sayan Biswas, Subhasish Sarkar, Pranesh Kumar, Priyadip Das, …
Proceedings of the National Academy of Sciences - PNAS, Vol.120(1), pp.e2213537120-e2213537120
01/03/2023
DOI: 10.1073/pnas.2213537120
PMCID: PMC9910480
PMID: 36574707
url
https://doi.org/10.1073/pnas.2213537120View
Published (Version of record) Open Access

Abstract

Dose-limiting cardiotoxicity remains a major limitation in the clinical use of cancer chemotherapeutics. Here, we describe a role for Regulator of G protein Signaling 7 (RGS7) in chemotherapy-dependent heart damage, the demonstration for a functional role of RGS7 outside of the nervous system and retina. Though expressed at low levels basally, we observed robust up-regulation of RGS7 in the human and murine myocardium following chemotherapy exposure. In ventricular cardiomyocytes (VCM), RGS7 forms a complex with Ca /calmodulin-dependent protein kinase (CaMKII) supported by key residues (K412 and P391) in the RGS domain of RGS7. In VCM treated with chemotherapeutic drugs, RGS7 facilitates CaMKII oxidation and phosphorylation and CaMKII-dependent oxidative stress, mitochondrial dysfunction, and apoptosis. Cardiac-specific RGS7 knockdown protected the heart against chemotherapy-dependent oxidative stress, fibrosis, and myocyte loss and improved left ventricular function in mice treated with doxorubicin. Conversely, RGS7 overexpression induced fibrosis, reactive oxygen species generation, and cell death in the murine myocardium that were mitigated following CaMKII inhibition. RGS7 also drives production and release of the cardiokine neuregulin-1, which facilitates paracrine communication between VCM and neighboring vascular endothelial cells (EC), a maladaptive mechanism contributing to VCM dysfunction in the failing heart. Importantly, while RGS7 was both necessary and sufficient to facilitate chemotherapy-dependent cytotoxicity in VCM, RGS7 is dispensable for the cancer-killing actions of these same drugs. These selective myocyte-intrinsic and myocyte-extrinsic actions of RGS7 in heart identify RGS7 as an attractive therapeutic target in the mitigation of chemotherapy-driven cardiotoxicity.
Animals Antineoplastic Agents - adverse effects Calcium-Calmodulin-Dependent Protein Kinase Type 2 - genetics Calcium-Calmodulin-Dependent Protein Kinase Type 2 - metabolism Cardiotoxicity - metabolism Endothelial Cells - metabolism Fibrosis Humans Mice Myocytes, Cardiac - metabolism RGS Proteins - genetics RGS Proteins - metabolism

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