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Gamma-interferon-inducible lysosomal thiol reductase maintains cardiac immuno-metabolic homeostasis in heart failure
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Gamma-interferon-inducible lysosomal thiol reductase maintains cardiac immuno-metabolic homeostasis in heart failure

Mark Li, Jinxi Wang, Qingwen Qian, Biyi Chen, Zeyuan Zhang, Elizabeth Barroso, Yuan Zhang, Duan Hall, Evan Abel, Long-Sheng Song, …
bioRxiv
Cold Spring Harbor Laboratory Press
02/22/2023
DOI: 10.1101/2022.07.03.498477
url
https://doi.org/10.1101/2022.07.03.498477View
Preprint (Author's original)This preprint has not been evaluated by subject experts through peer review. Preprints may undergo extensive changes and/or become peer-reviewed journal articles. Open Access

Abstract

Background: The lysosome is a central player in maintaining immuno-metabolic homeostasis. However, mechanistic insights into the regulation of lysosome-dependent immuno-metabolism in the heart are lacking. Lysosomal reductase Gamma Interferon-Inducible Thiol Reductase (GILT) is the only identified lysosomal reductase that controls diverse sets of lysosomal enzymes and cargoes. Methods: The role of cardiac GILT was assessed by generating a novel genetic mouse model and employing a multidisciplinary approach including surgical interventions, live in situ high resolution microscopy, whole-tissue respirometry analysis, unbiased transcriptomic and metabolomic analyses, and various cell biology and biochemical assays. Results: We found that expression and activity of GILT are reduced in hearts from humans and mice with heart failure (HF). Mice with cardiac specific loss of GILT develop late onset systolic HF at baseline. In the setting of nutrient-overload and experimental left ventricular pressure overload conditions, loss of GILT in cardiomyocytes accelerates the development of heart dysfunction. Transcriptomic and metabolic analyses further revealed that cardiac GILT deficiency alters adaptive immuno-metabolic signatures in the heart. Finally, at the cellular level, cardiac GILT deletion impaired mitochondrial respiration, which was in part due to NLR Family Pyrin Domain Containing 3 (NLRP3)-mediated elevation of mitochondrial oxidative stress. Conclusions: Together, these findings identify a causal link between a lysosome-inflammation axis, mitochondrial function and heart failure. Elucidation of these mechanisms will identify novel therapeutic strategies for treating HF. Competing Interest Statement The authors have declared no competing interest. Footnotes * This version of the manuscript has been revised to update our new data.
Heart Diseases Heart Failure Metabolism Oxidative Stress Cardiomyocytes Congestive heart failure Homeostasis Lysosomal enzymes Metabolomics Mitochondria Pyrin protein Thiol reductase Transcriptomics Ventricle γ-Interferon

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