RNA editing of Filamin A pre‐mRNA regulates vascular contraction and diastolic blood pressure

Epitranscriptomic events such as adenosine‐to‐inosine (A‐to‐I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that encodes actin crosslinking protein Filamin A (FLNA) mediates a Q‐to‐R transition in the interactive C‐terminal region. While FLNA editing is conse...

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Published inThe EMBO journal Vol. 37; no. 19
Main Authors Jain, Mamta, Mann, Tomer D, Stulić, Maja, Rao, Shailaja P, Kirsch, Andrijana, Pullirsch, Dieter, Strobl, Xué, Rath, Claus, Reissig, Lukas, Moreth, Kristin, Klein‐Rodewald, Tanja, Bekeredjian, Raffi, Gailus‐Durner, Valerie, Fuchs, Helmut, Hrabě de Angelis, Martin, Pablik, Eleonore, Cimatti, Laura, Martin, David, Zinnanti, Jelena, Graier, Wolfgang F, Sibilia, Maria, Frank, Saša, Levanon, Erez Y, Jantsch, Michael F
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.10.2018
Springer Nature B.V
John Wiley and Sons Inc
Subjects
Actin
Adenosine
adenosine deaminases acting on RNA (ADAR)
Animals
Aorta
Blood Pressure
Cardiovascular disease
Cardiovascular diseases
Cardiovascular system
Central nervous system
Coronary artery disease
Crosslinking
Disease control
Editing
EMBO11
EMBO36
EMBO46
Filamin A (FLNA)
Filamins - genetics
Filamins - metabolism
Heart diseases
Heart Ventricles - metabolism
Heart Ventricles - pathology
Humans
Hypertension
Hypertension - genetics
Hypertension - metabolism
Hypertension - pathology
Mice
mRNA
Muscle Contraction
Muscles
Myocardium - metabolism
Myocardium - pathology
Myosin
Phosphorylation
Pressure dependence
Proteins
Ribonucleic acid
RNA
RNA Editing
RNA modification
RNA Precursors - genetics
RNA Precursors - metabolism
Sequence Analysis, RNA
Smooth muscle
Substrates
Thickening
Vascular Remodeling
Ventricle
Vertebrates
cardiovascular disease
RNA editing
Filamin A (FLNA)
hypertension
adenosine deaminases acting on RNA (ADAR)
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Abstract Epitranscriptomic events such as adenosine‐to‐inosine (A‐to‐I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that encodes actin crosslinking protein Filamin A (FLNA) mediates a Q‐to‐R transition in the interactive C‐terminal region. While FLNA editing is conserved among vertebrates, its physiological function remains unclear. Here, we show that cardiovascular tissues in humans and mice show massive editing and that FLNA RNA is the most prominent substrate. Patient‐derived RNA‐Seq data demonstrate a significant drop in FLNA editing associated with cardiovascular diseases. Using mice with only impaired FLNA editing, we observed increased vascular contraction and diastolic hypertension accompanied by increased myosin light chain phosphorylation, arterial remodeling, and left ventricular wall thickening, which eventually causes cardiac remodeling and reduced systolic output. These results demonstrate a causal relationship between RNA editing and the development of cardiovascular disease indicating that a single epitranscriptomic RNA modification can maintain cardiovascular health. Synopsis RNA‐editing of Filamin A pre‐mRNA is decreased in human cardiac disease. A mouse model lacking this editing site shows altered smooth muscle contraction and diastolic blood pressure, illustrating that ADAR2‐dependent RNA editing plays a functional role outside the central nervous system. The Filamin A (FLNA) pre‐mRNA is subject to RNA editing with the highest rates seen in the cardiovascular system. FLNA editing rates are reduced in cardiovascular disease patients. In mice, FLNA editing controls smooth muscle contraction of the dorsal aorta. Mice deficient in FLNA editing show elevated diastolic blood pressure and cardiac remodeling. Graphical Abstract Disrupting a single mRNA editing site in mice affects smooth muscle contraction and diastolic blood pressure, while reduced editing at the same site in human correlates with cardiac disease.
AbstractList Epitranscriptomic events such as adenosine‐to‐inosine (A‐to‐I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that encodes actin crosslinking protein Filamin A (FLNA) mediates a Q‐to‐R transition in the interactive C‐terminal region. While FLNA editing is conserved among vertebrates, its physiological function remains unclear. Here, we show that cardiovascular tissues in humans and mice show massive editing and that FLNA RNA is the most prominent substrate. Patient‐derived RNA‐Seq data demonstrate a significant drop in FLNA editing associated with cardiovascular diseases. Using mice with only impaired FLNA editing, we observed increased vascular contraction and diastolic hypertension accompanied by increased myosin light chain phosphorylation, arterial remodeling, and left ventricular wall thickening, which eventually causes cardiac remodeling and reduced systolic output. These results demonstrate a causal relationship between RNA editing and the development of cardiovascular disease indicating that a single epitranscriptomic RNA modification can maintain cardiovascular health. Synopsis RNA‐editing of Filamin A pre‐mRNA is decreased in human cardiac disease. A mouse model lacking this editing site shows altered smooth muscle contraction and diastolic blood pressure, illustrating that ADAR2‐dependent RNA editing plays a functional role outside the central nervous system. The Filamin A (FLNA) pre‐mRNA is subject to RNA editing with the highest rates seen in the cardiovascular system. FLNA editing rates are reduced in cardiovascular disease patients. In mice, FLNA editing controls smooth muscle contraction of the dorsal aorta. Mice deficient in FLNA editing show elevated diastolic blood pressure and cardiac remodeling. Disrupting a single mRNA editing site in mice affects smooth muscle contraction and diastolic blood pressure, while reduced editing at the same site in human correlates with cardiac disease.
Epitranscriptomic events such as adenosine‐to‐inosine (A‐to‐I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that encodes actin crosslinking protein Filamin A (FLNA) mediates a Q‐to‐R transition in the interactive C‐terminal region. While FLNA editing is conserved among vertebrates, its physiological function remains unclear. Here, we show that cardiovascular tissues in humans and mice show massive editing and that FLNA RNA is the most prominent substrate. Patient‐derived RNA‐Seq data demonstrate a significant drop in FLNA editing associated with cardiovascular diseases. Using mice with only impaired FLNA editing, we observed increased vascular contraction and diastolic hypertension accompanied by increased myosin light chain phosphorylation, arterial remodeling, and left ventricular wall thickening, which eventually causes cardiac remodeling and reduced systolic output. These results demonstrate a causal relationship between RNA editing and the development of cardiovascular disease indicating that a single epitranscriptomic RNA modification can maintain cardiovascular health.
Epitranscriptomic events such as adenosine-to-inosine (A-to-I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that encodes actin crosslinking protein Filamin A (FLNA) mediates a Q-to-R transition in the interactive C-terminal region. While FLNA editing is conserved among vertebrates, its physiological function remains unclear. Here, we show that cardiovascular tissues in humans and mice show massive editing and that FLNA RNA is the most prominent substrate. Patient-derived RNA-Seq data demonstrate a significant drop in FLNA editing associated with cardiovascular diseases. Using mice with only impaired FLNA editing, we observed increased vascular contraction and diastolic hypertension accompanied by increased myosin light chain phosphorylation, arterial remodeling, and left ventricular wall thickening, which eventually causes cardiac remodeling and reduced systolic output. These results demonstrate a causal relationship between RNA editing and the development of cardiovascular disease indicating that a single epitranscriptomic RNA modification can maintain cardiovascular health.Epitranscriptomic events such as adenosine-to-inosine (A-to-I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that encodes actin crosslinking protein Filamin A (FLNA) mediates a Q-to-R transition in the interactive C-terminal region. While FLNA editing is conserved among vertebrates, its physiological function remains unclear. Here, we show that cardiovascular tissues in humans and mice show massive editing and that FLNA RNA is the most prominent substrate. Patient-derived RNA-Seq data demonstrate a significant drop in FLNA editing associated with cardiovascular diseases. Using mice with only impaired FLNA editing, we observed increased vascular contraction and diastolic hypertension accompanied by increased myosin light chain phosphorylation, arterial remodeling, and left ventricular wall thickening, which eventually causes cardiac remodeling and reduced systolic output. These results demonstrate a causal relationship between RNA editing and the development of cardiovascular disease indicating that a single epitranscriptomic RNA modification can maintain cardiovascular health.
Epitranscriptomic events such as adenosine‐to‐inosine (A‐to‐I) RNA editing by ADAR can recode mRNA s to translate novel proteins. Editing of the mRNA that encodes actin crosslinking protein Filamin A ( FLNA ) mediates a Q‐to‐R transition in the interactive C‐terminal region. While FLNA editing is conserved among vertebrates, its physiological function remains unclear. Here, we show that cardiovascular tissues in humans and mice show massive editing and that FLNA RNA is the most prominent substrate. Patient‐derived RNA ‐Seq data demonstrate a significant drop in FLNA editing associated with cardiovascular diseases. Using mice with only impaired FLNA editing, we observed increased vascular contraction and diastolic hypertension accompanied by increased myosin light chain phosphorylation, arterial remodeling, and left ventricular wall thickening, which eventually causes cardiac remodeling and reduced systolic output. These results demonstrate a causal relationship between RNA editing and the development of cardiovascular disease indicating that a single epitranscriptomic RNA modification can maintain cardiovascular health.
Epitranscriptomic events such as adenosine‐to‐inosine (A‐to‐I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that encodes actin crosslinking protein Filamin A (FLNA) mediates a Q‐to‐R transition in the interactive C‐terminal region. While FLNA editing is conserved among vertebrates, its physiological function remains unclear. Here, we show that cardiovascular tissues in humans and mice show massive editing and that FLNA RNA is the most prominent substrate. Patient‐derived RNA‐Seq data demonstrate a significant drop in FLNA editing associated with cardiovascular diseases. Using mice with only impaired FLNA editing, we observed increased vascular contraction and diastolic hypertension accompanied by increased myosin light chain phosphorylation, arterial remodeling, and left ventricular wall thickening, which eventually causes cardiac remodeling and reduced systolic output. These results demonstrate a causal relationship between RNA editing and the development of cardiovascular disease indicating that a single epitranscriptomic RNA modification can maintain cardiovascular health. Synopsis RNA‐editing of Filamin A pre‐mRNA is decreased in human cardiac disease. A mouse model lacking this editing site shows altered smooth muscle contraction and diastolic blood pressure, illustrating that ADAR2‐dependent RNA editing plays a functional role outside the central nervous system. The Filamin A (FLNA) pre‐mRNA is subject to RNA editing with the highest rates seen in the cardiovascular system. FLNA editing rates are reduced in cardiovascular disease patients. In mice, FLNA editing controls smooth muscle contraction of the dorsal aorta. Mice deficient in FLNA editing show elevated diastolic blood pressure and cardiac remodeling. Graphical Abstract Disrupting a single mRNA editing site in mice affects smooth muscle contraction and diastolic blood pressure, while reduced editing at the same site in human correlates with cardiac disease.
Author Mann, Tomer D
Strobl, Xué
Bekeredjian, Raffi
Martin, David
Gailus‐Durner, Valerie
Jain, Mamta
Hrabě de Angelis, Martin
Cimatti, Laura
Jantsch, Michael F
Frank, Saša
Fuchs, Helmut
Kirsch, Andrijana
Pablik, Eleonore
Levanon, Erez Y
Sibilia, Maria
Pullirsch, Dieter
Klein‐Rodewald, Tanja
Moreth, Kristin
Rao, Shailaja P
Reissig, Lukas
Zinnanti, Jelena
Stulić, Maja
Rath, Claus
Graier, Wolfgang F
AuthorAffiliation 1 Division of Cell Biology Center for Anatomy and Cell Biology Medical University of Vienna Vienna Austria
4 Center of Molecular Medicine Institute of Molecular Biology and Biochemistry Medical University of Graz Graz Austria
9 Department of Experimental Genetics Center of Life and Food Sciences Weihenstephan Technische Universität München Freising‐Weihenstephan Germany
10 German Center for Diabetes Research (DZD) Neuherberg Germany
6 German Mouse Clinic Institute of Experimental Genetics Helmholtz Zentrum München Neuherberg Germany
7 Institute of Pathology Helmholtz Zentrum München Neuherberg Germany
12 Vienna Biocenter Core Facilities GmbH Vienna Austria
5 Division of Anatomy Center for Anatomy and Cell Biology Medical University of Vienna Vienna Austria
11 Section for Medical Statistics CeMSIIS Medical University of Vienna Vienna Austria
8 Department of Cardiology University of Heidelberg Heidelberg Germany
3 Tel Aviv Sourasky Medical Center Tel Aviv Israel
13 Department of Medicine I Comprehe
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– name: 7 Institute of Pathology Helmholtz Zentrum München Neuherberg Germany
– name: 8 Department of Cardiology University of Heidelberg Heidelberg Germany
– name: 3 Tel Aviv Sourasky Medical Center Tel Aviv Israel
– name: 6 German Mouse Clinic Institute of Experimental Genetics Helmholtz Zentrum München Neuherberg Germany
– name: 2 The Mina and Everard Goodman Faculty of Life Sciences Bar Ilan University Ramat‐Gan Israel
– name: 10 German Center for Diabetes Research (DZD) Neuherberg Germany
– name: 5 Division of Anatomy Center for Anatomy and Cell Biology Medical University of Vienna Vienna Austria
– name: 9 Department of Experimental Genetics Center of Life and Food Sciences Weihenstephan Technische Universität München Freising‐Weihenstephan Germany
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30087110$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright The Author(s) 2018
2018 The Authors. Published under the terms of the CC BY 4.0 license
2018 The Authors. Published under the terms of the CC BY 4.0 license.
2018 EMBO
Copyright_xml – notice: The Author(s) 2018
– notice: 2018 The Authors. Published under the terms of the CC BY 4.0 license
– notice: 2018 The Authors. Published under the terms of the CC BY 4.0 license.
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Issue 19
Keywords cardiovascular disease
RNA editing
Filamin A (FLNA)
hypertension
adenosine deaminases acting on RNA (ADAR)
Language English
License Attribution
2018 The Authors. Published under the terms of the CC BY 4.0 license.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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content type line 14
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These authors contributed equally to this work
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0000-0002-3641-4198
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SSID ssj0005871
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Snippet Epitranscriptomic events such as adenosine‐to‐inosine (A‐to‐I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that...
Epitranscriptomic events such as adenosine-to-inosine (A-to-I) RNA editing by ADAR can recode mRNAs to translate novel proteins. Editing of the mRNA that...
Epitranscriptomic events such as adenosine‐to‐inosine (A‐to‐I) RNA editing by ADAR can recode mRNA s to translate novel proteins. Editing of the mRNA that...
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SubjectTerms Actin
Adenosine
adenosine deaminases acting on RNA (ADAR)
Animals
Aorta
Blood Pressure
Cardiovascular disease
Cardiovascular diseases
Cardiovascular system
Central nervous system
Coronary artery disease
Crosslinking
Disease control
Editing
EMBO11
EMBO36
EMBO46
Filamin A (FLNA)
Filamins - genetics
Filamins - metabolism
Heart diseases
Heart Ventricles - metabolism
Heart Ventricles - pathology
Humans
Hypertension
Hypertension - genetics
Hypertension - metabolism
Hypertension - pathology
Mice
mRNA
Muscle Contraction
Muscles
Myocardium - metabolism
Myocardium - pathology
Myosin
Phosphorylation
Pressure dependence
Proteins
Ribonucleic acid
RNA
RNA Editing
RNA modification
RNA Precursors - genetics
RNA Precursors - metabolism
Sequence Analysis, RNA
Smooth muscle
Substrates
Thickening
Vascular Remodeling
Ventricle
Vertebrates
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Title RNA editing of Filamin A pre‐mRNA regulates vascular contraction and diastolic blood pressure
URI https://link.springer.com/article/10.15252/embj.201694813
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.201694813
https://www.ncbi.nlm.nih.gov/pubmed/30087110
https://www.proquest.com/docview/2114567097
https://www.proquest.com/docview/2085657871
https://pubmed.ncbi.nlm.nih.gov/PMC6166124
Volume 37
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