USP20 deletion promotes eccentric cardiac remodeling in response to pressure overload and increases mortality
- PMID: 39365672
- PMCID: PMC11559650
- DOI: 10.1152/ajpheart.00329.2024
USP20 deletion promotes eccentric cardiac remodeling in response to pressure overload and increases mortality
Abstract
Left ventricular hypertrophy (LVH) caused by chronic pressure overload with subsequent pathological remodeling is a major cardiovascular risk factor for heart failure and mortality. The role of deubiquitinases in LVH has not been well characterized. To define whether the deubiquitinase ubiquitin-specific peptidase 20 (USP20) regulates LVH, we subjected USP20 knockout (KO) and cognate wild-type (WT) mice to chronic pressure overload by transverse aortic constriction (TAC) and measured changes in cardiac function by serial echocardiography followed by histological and biochemical evaluations. USP20-KO mice showed severe deterioration of systolic function within 4 wk of TAC compared with WT cohorts. Both USP20-KO TAC and WT-TAC cohorts presented cardiac hypertrophy following pressure overload. However, USP20-KO-TAC mice showed an increase in cardiomyocyte length and developed maladaptive eccentric hypertrophy, a phenotype generally observed with volume overload states and decompensated heart failure. In contrast, WT-TAC mice displayed an increase in cardiomyocyte width, producing concentric remodeling that is characteristic of pressure overload. In addition, cardiomyocyte apoptosis, interstitial fibrosis, and mouse mortality were augmented in USP20-KO-TAC compared with WT-TAC mice. Quantitative mass spectrometry of LV tissue revealed that the expression of sarcomeric myosin heavy chain 7 (MYH7), a fetal gene normally upregulated during cardiac remodeling, was significantly reduced in USP20-KO after TAC. Mechanistically, we identified increased degradative lysine-48 polyubiquitination of MYH7 in USP20-KO hearts, indicating that USP20-mediated deubiquitination likely prevents protein degradation of MYH7 during pressure overload. Our findings suggest that USP20-dependent signaling pathways regulate the layering pattern of sarcomeres to suppress maladaptive remodeling during chronic pressure overload and prevent cardiac failure.NEW & NOTEWORTHY We identify ubiquitin-specific peptidase 20 (USP20) as an important enzyme that is required for cardiac homeostasis and function, particularly during myocardial pressure overload. USP20 regulates protein stability of cardiac MYH7, an essential molecular motor protein expressed in sarcomeres; loss-of-function mutations of MYH7 are associated with human hypertrophic cardiomyopathy, cardiac failure, and sudden death. Enhancing USP20 activity could be a potential therapeutic approach to prevent the development of maladaptive state of eccentric hypertrophy and heart failure.
Keywords: apoptosis; cardiac hypertrophy; deubiquitinase; eccentric hypertrophy; heart failure.
Conflict of interest statement
H.A.R. is a scientific cofounder of Trevena, Inc., a company that is developing GPCR-targeted therapeutics. None of the other authors has any conflicts of interest, financial or otherwise, to disclose.
Comment in
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The importance of myosin ubiquitination status for cardiac remodeling: USP20 has entered the chat.Am J Physiol Heart Circ Physiol. 2024 Nov 1;327(5):H1306-H1308. doi: 10.1152/ajpheart.00712.2024. Epub 2024 Oct 25. Am J Physiol Heart Circ Physiol. 2024. PMID: 39453432 No abstract available.
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The importance of myosin ubiquitination status for cardiac remodeling: USP20 has entered the chat.Am J Physiol Heart Circ Physiol. 2024 Nov 1;327(5):H1306-H1308. doi: 10.1152/ajpheart.00712.2024. Epub 2024 Oct 25. Am J Physiol Heart Circ Physiol. 2024. PMID: 39453432 No abstract available.
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