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Modulation of miR-29 influences myocardial compliance likely through coordinated regulation of calcium handling and extracellular matrix
Journal article   Open access   Peer reviewed

Modulation of miR-29 influences myocardial compliance likely through coordinated regulation of calcium handling and extracellular matrix

Xiaoming Zhang, Jared M. McLendon, Bailey D. Peck, Biyi Chen, Long-Sheng Song and Ryan L. Boudreau
Molecular therapy. Nucleic acids, Vol.34, 102081
12/12/2023
DOI: 10.1016/j.omtn.2023.102081
PMCID: PMC10726423
PMID: 38111915
url
https://doi.org/10.1016/j.omtn.2023.102081View
Published (Version of record) Open Access

Abstract

MicroRNAs (miRNAs) control the expression of diverse subsets of target mRNAs, and studies have found miRNA dysregulation in failing hearts. Expression of miR-29 is abundant in heart, increases with aging, and is altered in cardiomyopathies. Prior studies demonstrate that miR-29 reduction via genetic knockout or pharmacologic blockade can blunt cardiac hypertrophy and fibrosis in mice. Surprisingly, this depended on specifically blunting miR-29 actions in cardiomyocytes versus fibroblasts. To begin developing more translationally relevant vectors, we generated a novel transgene-encoded miR-29 inhibitor (TuD-29) that can be incorporated into a viral-mediated gene therapy for cardioprotection. Here, we corroborate that miR-29 expression and activity is higher in cardiomyocytes versus fibroblasts and demonstrate that TuD-29 effectively blunts hypertrophic responses in cultured cardiomyocytes and mouse hearts. Furthermore, we found that adeno-associated virus (AAV)–mediated miR-29 overexpression in mouse hearts induces early diastolic dysfunction, whereas AAV:TuD-29 treatment improves cardiac output by increasing end-diastolic and stroke volumes. The integration of RNA sequencing and miRNA-target interactomes reveals that miR-29 regulates genes involved in calcium handling, cell stress and hypertrophy, metabolism, ion transport, and extracellular matrix remodeling. These investigations support a likely versatile role for miR-29 in influencing myocardial compliance and relaxation, potentially providing a unique therapeutic avenue to improve diastolic function in heart failure patients. Boudreau and colleagues corroborate that miR-29 expression and function is higher in cardiac myocytes versus fibroblasts and promotes cardiomyocyte hypertrophy. In studies in mice, adeno-associated virus 9–mediated miR-29 overexpression impaired diastolic filling and cardiac output (CO), whereas miR-29 inhibition blunted pressure overload–induced hypertrophy and improved diastolic filling and CO.
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