AntimiR-21 Prevents Myocardial Dysfunction in a Pig Model of Ischemia/Reperfusion Injury.


Journal

Journal of the American College of Cardiology
ISSN: 1558-3597
Titre abrégé: J Am Coll Cardiol
Pays: United States
ID NLM: 8301365

Informations de publication

Date de publication:
21 04 2020
Historique:
received: 12 12 2019
revised: 05 02 2020
accepted: 10 02 2020
entrez: 18 4 2020
pubmed: 18 4 2020
medline: 29 12 2020
Statut: ppublish

Résumé

miR-21 is a central regulator of cardiac fibrosis, and its inhibition in small-animal models has been shown to be an effective antifibrotic strategy in various organs, including the heart. Effective delivery of therapeutic antisense micro-ribonucleic acid (antimiR) molecules to the myocardium in larger organisms is challenging, though, and remains to be established for models of chronic heart failure. The aims of this study were to test the applicability and therapeutic efficacy of local, catheter-based delivery of antimiR-21 in a pig model of heart failure and determine its effect on the cardiac transcriptomic signature and cellular composition. Pigs underwent transient percutaneous occlusion of the left coronary artery and were followed up for 33 days. AntimiR-21 (10 mg) was applied by intracoronary infusion at days 5 and 19 after the injury. Cardiac function was assessed in vivo, followed by histological analyses and deep ribonucleic acid sequencing (RNA-seq) of the myocardium and genetic deconvolution analysis. AntimiR-21 effectively suppressed the remodeling-associated increase of miR-21. At 33 days after ischemia/reperfusion injury, LNA-21-treated hearts exhibited reduced cardiac fibrosis and hypertrophy and improved cardiac function. Deep RNA-seq revealed a significant derepression of the miR-21 targetome in antimiR-21-treated myocardium and a suppression of the inflammatory response and mitogen-activated protein kinase signaling. A genetic deconvolution approach built on deep RNA-seq and single-cell RNA-seq data identified reductions in macrophage and fibroblast numbers as the key cell types affected by antimiR-21 treatment. This study provides the first evidence for the feasibility and therapeutic efficacy of miR-21 inhibition in a large animal model of heart failure.

Sections du résumé

BACKGROUND
miR-21 is a central regulator of cardiac fibrosis, and its inhibition in small-animal models has been shown to be an effective antifibrotic strategy in various organs, including the heart. Effective delivery of therapeutic antisense micro-ribonucleic acid (antimiR) molecules to the myocardium in larger organisms is challenging, though, and remains to be established for models of chronic heart failure.
OBJECTIVES
The aims of this study were to test the applicability and therapeutic efficacy of local, catheter-based delivery of antimiR-21 in a pig model of heart failure and determine its effect on the cardiac transcriptomic signature and cellular composition.
METHODS
Pigs underwent transient percutaneous occlusion of the left coronary artery and were followed up for 33 days. AntimiR-21 (10 mg) was applied by intracoronary infusion at days 5 and 19 after the injury. Cardiac function was assessed in vivo, followed by histological analyses and deep ribonucleic acid sequencing (RNA-seq) of the myocardium and genetic deconvolution analysis.
RESULTS
AntimiR-21 effectively suppressed the remodeling-associated increase of miR-21. At 33 days after ischemia/reperfusion injury, LNA-21-treated hearts exhibited reduced cardiac fibrosis and hypertrophy and improved cardiac function. Deep RNA-seq revealed a significant derepression of the miR-21 targetome in antimiR-21-treated myocardium and a suppression of the inflammatory response and mitogen-activated protein kinase signaling. A genetic deconvolution approach built on deep RNA-seq and single-cell RNA-seq data identified reductions in macrophage and fibroblast numbers as the key cell types affected by antimiR-21 treatment.
CONCLUSIONS
This study provides the first evidence for the feasibility and therapeutic efficacy of miR-21 inhibition in a large animal model of heart failure.

Identifiants

pubmed: 32299591
pii: S0735-1097(20)34416-8
doi: 10.1016/j.jacc.2020.02.041
pii:
doi:

Substances chimiques

MIRN21 microRNA, human 0
MicroRNAs 0
Oligonucleotides 0
locked nucleic acid 0
Mitogen-Activated Protein Kinases EC 2.7.11.24

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1788-1800

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Rabea Hinkel (R)

1. Medizinische Klinik und Poliklinik, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany; Institute for Cardiovascular Prevention, Ludwigs-Maximilians-Universität München, Munich, Germany; Deutsches Primatenzentrum GmbH, Leibnitz-Institut für Primatenforschung, Laboratory Animal Science Unit, Göttingen, Germany; DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany.

Deepak Ramanujam (D)

DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany; Institut für Pharmakologie und Toxikologie, Technische Universität München, Munich, Germany.

Veronika Kaczmarek (V)

1. Medizinische Klinik und Poliklinik, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany; Institute for Cardiovascular Prevention, Ludwigs-Maximilians-Universität München, Munich, Germany.

Andrea Howe (A)

1. Medizinische Klinik und Poliklinik, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany; Institute for Cardiovascular Prevention, Ludwigs-Maximilians-Universität München, Munich, Germany.

Katharina Klett (K)

1. Medizinische Klinik und Poliklinik, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany; Institute for Cardiovascular Prevention, Ludwigs-Maximilians-Universität München, Munich, Germany.

Christina Beck (C)

DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany; Institut für Pharmakologie und Toxikologie, Technische Universität München, Munich, Germany.

Anne Dueck (A)

DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany; Institut für Pharmakologie und Toxikologie, Technische Universität München, Munich, Germany.

Thomas Thum (T)

Institute of Molecular and Translational Therapeutic Strategies, Hannover Medical School, Hannover, Germany.

Karl-Ludwig Laugwitz (KL)

1. Medizinische Klinik und Poliklinik, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany; DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany.

Lars Maegdefessel (L)

DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany; Department of Vascular Surgery, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany.

Christian Weber (C)

Institute for Cardiovascular Prevention, Ludwigs-Maximilians-Universität München, Munich, Germany; DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany; Department of Biochemistry, Cardiovascular Research Institute Maastricht, Maastricht University, Maastricht, the Netherlands.

Christian Kupatt (C)

1. Medizinische Klinik und Poliklinik, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany; DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany. Electronic address: christian.kupatt@tum.de.

Stefan Engelhardt (S)

DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany; Institut für Pharmakologie und Toxikologie, Technische Universität München, Munich, Germany. Electronic address: stefan.engelhardt@tum.de.

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