RNA mis‐splicing in children with congenital myotonic dystrophy is associated with physical function

Abstract Objectives Dysregulated RNA alternative splicing is the hallmark of myotonic dystrophy type 1 (DM1). However, the association between RNA mis‐splicing and physical function in children with the most severe form of disease, congenital myotonic dystrophy (CDM), is unknown. Methods Eighty‐two...

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Main Authors: Julia M. Hartman, Kobe Ikegami, Marina Provenzano, Kameron Bates, Amanda Butler, Aileen S. Jones, Kiera N. Berggren, Jeanne Dekdebrun, Marnee J. McKay, Jennifer N. Baldwin, Kayla M. D. Cornett, Joshua Burns, Michael Kiefer, Nicholas E. Johnson, Melissa A. Hale, the DMCRN Consortium
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Annals of Clinical and Translational Neurology
Online Access:https://doi.org/10.1002/acn3.52224
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author Julia M. Hartman
Kobe Ikegami
Marina Provenzano
Kameron Bates
Amanda Butler
Aileen S. Jones
Kiera N. Berggren
Jeanne Dekdebrun
Marnee J. McKay
Jennifer N. Baldwin
Kayla M. D. Cornett
Joshua Burns
Michael Kiefer
Nicholas E. Johnson
Melissa A. Hale
the DMCRN Consortium
author_facet Julia M. Hartman
Kobe Ikegami
Marina Provenzano
Kameron Bates
Amanda Butler
Aileen S. Jones
Kiera N. Berggren
Jeanne Dekdebrun
Marnee J. McKay
Jennifer N. Baldwin
Kayla M. D. Cornett
Joshua Burns
Michael Kiefer
Nicholas E. Johnson
Melissa A. Hale
the DMCRN Consortium
author_sort Julia M. Hartman
collection DOAJ
description Abstract Objectives Dysregulated RNA alternative splicing is the hallmark of myotonic dystrophy type 1 (DM1). However, the association between RNA mis‐splicing and physical function in children with the most severe form of disease, congenital myotonic dystrophy (CDM), is unknown. Methods Eighty‐two participants (42 adults with DM1 and 40 children with CDM) with muscle biopsies and measures of myotonia, motor function, and strength were combined from five observational studies. Data were normalized and correlated with an aggregate measure of alternative splicing dysregulation, [MBNL]inferred, in skeletal muscle biopsies. Multiple linear regression analysis was performed to predict [MBNL]inferred using clinical outcome measures alone. Similar analyses were performed to predict 12‐month physical function using baseline metrics. Results Myotonia (measured via vHOT) was significantly correlated with RNA mis‐splicing in our cross‐sectional population of all DM1 individuals; CDM participants alone displayed no myotonia despite a similar range of RNA mis‐splicing. Measures of motor performance and muscle strength were significantly associated with [MBNL]inferred in our cohort of all DM1 individuals and when assessing children with CDM independently. Multiple linear regression analyses yielded two models capable of predicting [MBNL]inferred from select clinical outcome assessments alone in all subjects (adjusted R2 = 0.6723) or exclusively in children with CDM (adjusted R2 = 0.5875). Interpretation Our findings establish significant correlations between skeletal muscle performance and a composite measure of alternative splicing dysregulation, [MBNL]inferred, in DM1. The strength of these correlations and the development of predictive models will assist in designing efficacious clinical trials for individuals with DM1, particularly CDM.
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spelling doaj-art-39ea475afc2640619fc2a601ba893d7c2024-12-17T16:12:21ZengWileyAnnals of Clinical and Translational Neurology2328-95032024-12-0111123175319110.1002/acn3.52224RNA mis‐splicing in children with congenital myotonic dystrophy is associated with physical functionJulia M. Hartman0Kobe Ikegami1Marina Provenzano2Kameron Bates3Amanda Butler4Aileen S. Jones5Kiera N. Berggren6Jeanne Dekdebrun7Marnee J. McKay8Jennifer N. Baldwin9Kayla M. D. Cornett10Joshua Burns11Michael Kiefer12Nicholas E. Johnson13Melissa A. Hale14the DMCRN ConsortiumMedical Scientist Training Program Virginia Commonwealth University Richmond Virginia 23298 USACenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USACenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USACenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USACenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USACenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USACenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USADepartment of Neurology University of Rochester School of Medicine and Dentistry Rochester New York 14642 USASydney School of Health Sciences, Faculty of Medicine and Health The University of Sydney Sydney New South Wales 2006 AustraliaSydney School of Health Sciences, Faculty of Medicine and Health The University of Sydney Sydney New South Wales 2006 AustraliaSydney School of Health Sciences, Faculty of Medicine and Health The University of Sydney Sydney New South Wales 2006 AustraliaSydney School of Health Sciences, Faculty of Medicine and Health The University of Sydney Sydney New South Wales 2006 AustraliaCenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USACenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USACenter for Inherited Myology Research Virginia Commonwealth University Richmond Virginia 23298 USAAbstract Objectives Dysregulated RNA alternative splicing is the hallmark of myotonic dystrophy type 1 (DM1). However, the association between RNA mis‐splicing and physical function in children with the most severe form of disease, congenital myotonic dystrophy (CDM), is unknown. Methods Eighty‐two participants (42 adults with DM1 and 40 children with CDM) with muscle biopsies and measures of myotonia, motor function, and strength were combined from five observational studies. Data were normalized and correlated with an aggregate measure of alternative splicing dysregulation, [MBNL]inferred, in skeletal muscle biopsies. Multiple linear regression analysis was performed to predict [MBNL]inferred using clinical outcome measures alone. Similar analyses were performed to predict 12‐month physical function using baseline metrics. Results Myotonia (measured via vHOT) was significantly correlated with RNA mis‐splicing in our cross‐sectional population of all DM1 individuals; CDM participants alone displayed no myotonia despite a similar range of RNA mis‐splicing. Measures of motor performance and muscle strength were significantly associated with [MBNL]inferred in our cohort of all DM1 individuals and when assessing children with CDM independently. Multiple linear regression analyses yielded two models capable of predicting [MBNL]inferred from select clinical outcome assessments alone in all subjects (adjusted R2 = 0.6723) or exclusively in children with CDM (adjusted R2 = 0.5875). Interpretation Our findings establish significant correlations between skeletal muscle performance and a composite measure of alternative splicing dysregulation, [MBNL]inferred, in DM1. The strength of these correlations and the development of predictive models will assist in designing efficacious clinical trials for individuals with DM1, particularly CDM.https://doi.org/10.1002/acn3.52224
spellingShingle Julia M. Hartman
Kobe Ikegami
Marina Provenzano
Kameron Bates
Amanda Butler
Aileen S. Jones
Kiera N. Berggren
Jeanne Dekdebrun
Marnee J. McKay
Jennifer N. Baldwin
Kayla M. D. Cornett
Joshua Burns
Michael Kiefer
Nicholas E. Johnson
Melissa A. Hale
the DMCRN Consortium
RNA mis‐splicing in children with congenital myotonic dystrophy is associated with physical function
Annals of Clinical and Translational Neurology
title RNA mis‐splicing in children with congenital myotonic dystrophy is associated with physical function
title_full RNA mis‐splicing in children with congenital myotonic dystrophy is associated with physical function
title_fullStr RNA mis‐splicing in children with congenital myotonic dystrophy is associated with physical function
title_full_unstemmed RNA mis‐splicing in children with congenital myotonic dystrophy is associated with physical function
title_short RNA mis‐splicing in children with congenital myotonic dystrophy is associated with physical function
title_sort rna mis splicing in children with congenital myotonic dystrophy is associated with physical function
url https://doi.org/10.1002/acn3.52224
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