Compound loss of muscleblind‐like function in myotonic dystrophy

Abstract Myotonic dystrophy (DM) is a multi‐systemic disease that impacts cardiac and skeletal muscle as well as the central nervous system (CNS). DM is unusual because it is an RNA‐mediated disorder due to the expression of toxic microsatellite expansion RNAs that alter the activities of RNA proces...

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Main Authors: Kuang‐Yung Lee, Moyi Li, Mini Manchanda, Ranjan Batra, Konstantinos Charizanis, Apoorva Mohan, Sonisha A. Warren, Christopher M. Chamberlain, Dustin Finn, Hannah Hong, Hassan Ashraf, Hideko Kasahara, Laura P. W. Ranum, Maurice S. Swanson
Format: Article
Language:English
Published: Springer Nature 2013-10-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.1002/emmm.201303275
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author Kuang‐Yung Lee
Moyi Li
Mini Manchanda
Ranjan Batra
Konstantinos Charizanis
Apoorva Mohan
Sonisha A. Warren
Christopher M. Chamberlain
Dustin Finn
Hannah Hong
Hassan Ashraf
Hideko Kasahara
Laura P. W. Ranum
Maurice S. Swanson
author_facet Kuang‐Yung Lee
Moyi Li
Mini Manchanda
Ranjan Batra
Konstantinos Charizanis
Apoorva Mohan
Sonisha A. Warren
Christopher M. Chamberlain
Dustin Finn
Hannah Hong
Hassan Ashraf
Hideko Kasahara
Laura P. W. Ranum
Maurice S. Swanson
author_sort Kuang‐Yung Lee
collection DOAJ
description Abstract Myotonic dystrophy (DM) is a multi‐systemic disease that impacts cardiac and skeletal muscle as well as the central nervous system (CNS). DM is unusual because it is an RNA‐mediated disorder due to the expression of toxic microsatellite expansion RNAs that alter the activities of RNA processing factors, including the muscleblind‐like (MBNL) proteins. While these mutant RNAs inhibit MBNL1 splicing activity in heart and skeletal muscles, Mbnl1 knockout mice fail to recapitulate the full‐range of DM symptoms in these tissues. Here, we generate mouse Mbnl compound knockouts to test the hypothesis that Mbnl2 functionally compensates for Mbnl1 loss. Although Mbnl1−/−; Mbnl2−/− double knockouts (DKOs) are embryonic lethal, Mbnl1−/−; Mbnl2+/− mice are viable but develop cardinal features of DM muscle disease including reduced lifespan, heart conduction block, severe myotonia and progressive skeletal muscle weakness. Mbnl2 protein levels are elevated in Mbnl1−/− knockouts where Mbnl2 targets Mbnl1‐regulated exons. These findings support the hypothesis that compound loss of MBNL function is a critical event in DM pathogenesis and provide novel mouse models to investigate additional pathways disrupted in this RNA‐mediated disease.
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spelling doaj-art-e6ecfc7eb11f40d5b72afc0761cf559b2025-08-20T02:11:26ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842013-10-015121887190010.1002/emmm.201303275Compound loss of muscleblind‐like function in myotonic dystrophyKuang‐Yung Lee0Moyi Li1Mini Manchanda2Ranjan Batra3Konstantinos Charizanis4Apoorva Mohan5Sonisha A. Warren6Christopher M. Chamberlain7Dustin Finn8Hannah Hong9Hassan Ashraf10Hideko Kasahara11Laura P. W. Ranum12Maurice S. Swanson13Department of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Physiology and Functional Genomics, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Physiology and Functional Genomics, University of Florida, College of MedicineDepartment of Physiology and Functional Genomics, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineDepartment of Molecular Genetics and Microbiology, Center for NeuroGenetics and the Genetics Institute, University of Florida, College of MedicineAbstract Myotonic dystrophy (DM) is a multi‐systemic disease that impacts cardiac and skeletal muscle as well as the central nervous system (CNS). DM is unusual because it is an RNA‐mediated disorder due to the expression of toxic microsatellite expansion RNAs that alter the activities of RNA processing factors, including the muscleblind‐like (MBNL) proteins. While these mutant RNAs inhibit MBNL1 splicing activity in heart and skeletal muscles, Mbnl1 knockout mice fail to recapitulate the full‐range of DM symptoms in these tissues. Here, we generate mouse Mbnl compound knockouts to test the hypothesis that Mbnl2 functionally compensates for Mbnl1 loss. Although Mbnl1−/−; Mbnl2−/− double knockouts (DKOs) are embryonic lethal, Mbnl1−/−; Mbnl2+/− mice are viable but develop cardinal features of DM muscle disease including reduced lifespan, heart conduction block, severe myotonia and progressive skeletal muscle weakness. Mbnl2 protein levels are elevated in Mbnl1−/− knockouts where Mbnl2 targets Mbnl1‐regulated exons. These findings support the hypothesis that compound loss of MBNL function is a critical event in DM pathogenesis and provide novel mouse models to investigate additional pathways disrupted in this RNA‐mediated disease.https://doi.org/10.1002/emmm.201303275Mbnl1Mbnl2muscleblind‐likemyotonic dystrophyRNA‐mediated disease
spellingShingle Kuang‐Yung Lee
Moyi Li
Mini Manchanda
Ranjan Batra
Konstantinos Charizanis
Apoorva Mohan
Sonisha A. Warren
Christopher M. Chamberlain
Dustin Finn
Hannah Hong
Hassan Ashraf
Hideko Kasahara
Laura P. W. Ranum
Maurice S. Swanson
Compound loss of muscleblind‐like function in myotonic dystrophy
EMBO Molecular Medicine
Mbnl1
Mbnl2
muscleblind‐like
myotonic dystrophy
RNA‐mediated disease
title Compound loss of muscleblind‐like function in myotonic dystrophy
title_full Compound loss of muscleblind‐like function in myotonic dystrophy
title_fullStr Compound loss of muscleblind‐like function in myotonic dystrophy
title_full_unstemmed Compound loss of muscleblind‐like function in myotonic dystrophy
title_short Compound loss of muscleblind‐like function in myotonic dystrophy
title_sort compound loss of muscleblind like function in myotonic dystrophy
topic Mbnl1
Mbnl2
muscleblind‐like
myotonic dystrophy
RNA‐mediated disease
url https://doi.org/10.1002/emmm.201303275
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