Repurposed Nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of Duchenne muscular dystrophy

In inherited neuromuscular disease, Duchenne muscular dystrophy (DMD), glucocorticoids significantly slow disease progression yet impart side effects severe enough to preclude use in a significant proportion of patients. Extending our findings that acute treatment with FDA approved multiple sclerosi...

Full description

Saved in:
Bibliographic Details
Main Authors: Stephanie Kourakis, Cara A. Timpani, Ryan M. Bagaric, Bo Qi, Benazir A. Ali, Rebecca Boyer, Guinevere Spiesberger, Nitika Kandhari, Xu Yan, Jujiao Kuang, Ankita Tulangekar, Judy B. de Haan, Deanna Deveson-Lucas, Nicole Stupka, Dirk Fischer, Emma Rybalka
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Redox Biology
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213231725001892
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850133716599308288
author Stephanie Kourakis
Cara A. Timpani
Ryan M. Bagaric
Bo Qi
Benazir A. Ali
Rebecca Boyer
Guinevere Spiesberger
Nitika Kandhari
Xu Yan
Jujiao Kuang
Ankita Tulangekar
Judy B. de Haan
Deanna Deveson-Lucas
Nicole Stupka
Dirk Fischer
Emma Rybalka
author_facet Stephanie Kourakis
Cara A. Timpani
Ryan M. Bagaric
Bo Qi
Benazir A. Ali
Rebecca Boyer
Guinevere Spiesberger
Nitika Kandhari
Xu Yan
Jujiao Kuang
Ankita Tulangekar
Judy B. de Haan
Deanna Deveson-Lucas
Nicole Stupka
Dirk Fischer
Emma Rybalka
author_sort Stephanie Kourakis
collection DOAJ
description In inherited neuromuscular disease, Duchenne muscular dystrophy (DMD), glucocorticoids significantly slow disease progression yet impart side effects severe enough to preclude use in a significant proportion of patients. Extending our findings that acute treatment with FDA approved multiple sclerosis drug, dimethyl fumarate (DMF), rescues muscle pathology in juvenile mdx mice, we aimed to conduct tiered pre-clinical testing toward translation. To aggravate disease phenotype in adult mdx muscles that usually lack human equivalent muscle pathology, we used bi-weekly treadmill running for 4 weeks which increased plasma DMD biomarker, creatine kinase, by 2-fold and quadriceps fibrosis by ∼30 %. Using this model, we screened DMF for 5 weeks in a head-to-head comparison, and in combination, with standard-of-care prednisone (PRED), to model the most likely clinical trial scenario. We show comparable efficacy between DMF and PRED at reducing inflammation via NF-κB suppression and CD68+ macrophage infiltration. Moderate term DMF monotherapy had additional anti-fibrotic and anti-lipogenic effects on skeletal and cardiac muscle beyond those seen with PRED treatment, although combination therapy exacerbated fibrosis in quadriceps. Our study supports DMF as a repurposing candidate for DMD, especially for patients who cannot tolerate chronic glucocorticoid treatment. We also highlight the importance of evaluating combination therapy to identify potential off-target effects between emerging therapeutics and glucocorticoids towards better designed clinical trials.
format Article
id doaj-art-d5089dfe55b743d8939e5e10cdcdb3ce
institution OA Journals
issn 2213-2317
language English
publishDate 2025-07-01
publisher Elsevier
record_format Article
series Redox Biology
spelling doaj-art-d5089dfe55b743d8939e5e10cdcdb3ce2025-08-20T02:31:54ZengElsevierRedox Biology2213-23172025-07-018410367610.1016/j.redox.2025.103676Repurposed Nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of Duchenne muscular dystrophyStephanie Kourakis0Cara A. Timpani1Ryan M. Bagaric2Bo Qi3Benazir A. Ali4Rebecca Boyer5Guinevere Spiesberger6Nitika Kandhari7Xu Yan8Jujiao Kuang9Ankita Tulangekar10Judy B. de Haan11Deanna Deveson-Lucas12Nicole Stupka13Dirk Fischer14Emma Rybalka15Institute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Inherited and Acquired Myopathies Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Inherited and Acquired Myopathies Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, Australia; Department of Medicine – Western Health, Melbourne Medical School, The University of Melbourne, St Albans, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Inherited and Acquired Myopathies Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Inherited and Acquired Myopathies Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Inherited and Acquired Myopathies Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Inherited and Acquired Myopathies Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, AustraliaMonash Genomics and Bioinformatics Platform, Biomedical Discovery Institute, Monash University, Clayton, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Sarcopenia Research Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, AustraliaInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Inherited and Acquired Myopathies Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, AustraliaBasic Science Domain, Oxidative Stress Laboratory, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia; Baker Department of Cardiometabolic Health, University of Melbourne, Parkville, Victoria, AustraliaMonash Genomics and Bioinformatics Platform, Biomedical Discovery Institute, Monash University, Clayton, Victoria, AustraliaDepartment of Medicine – Western Health, Melbourne Medical School, The University of Melbourne, St Albans, Victoria, Australia; Institute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, AustraliaDivision of Neuropediatric and Developmental Medicine, University Children's Hospital of Basel (UKBB), Basel, SwitzerlandInstitute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia; Inherited and Acquired Myopathies Program, Australian Institute for Musculoskeletal Science (AIMSS), St Albans, Victoria, Australia; Corresponding author. Institute for Health and Sport (IHeS), Victoria University, Melbourne, Victoria, Australia.In inherited neuromuscular disease, Duchenne muscular dystrophy (DMD), glucocorticoids significantly slow disease progression yet impart side effects severe enough to preclude use in a significant proportion of patients. Extending our findings that acute treatment with FDA approved multiple sclerosis drug, dimethyl fumarate (DMF), rescues muscle pathology in juvenile mdx mice, we aimed to conduct tiered pre-clinical testing toward translation. To aggravate disease phenotype in adult mdx muscles that usually lack human equivalent muscle pathology, we used bi-weekly treadmill running for 4 weeks which increased plasma DMD biomarker, creatine kinase, by 2-fold and quadriceps fibrosis by ∼30 %. Using this model, we screened DMF for 5 weeks in a head-to-head comparison, and in combination, with standard-of-care prednisone (PRED), to model the most likely clinical trial scenario. We show comparable efficacy between DMF and PRED at reducing inflammation via NF-κB suppression and CD68+ macrophage infiltration. Moderate term DMF monotherapy had additional anti-fibrotic and anti-lipogenic effects on skeletal and cardiac muscle beyond those seen with PRED treatment, although combination therapy exacerbated fibrosis in quadriceps. Our study supports DMF as a repurposing candidate for DMD, especially for patients who cannot tolerate chronic glucocorticoid treatment. We also highlight the importance of evaluating combination therapy to identify potential off-target effects between emerging therapeutics and glucocorticoids towards better designed clinical trials.http://www.sciencedirect.com/science/article/pii/S2213231725001892Duchenne muscular dystrophyDimethyl fumarateTherapeuticsMuscle pathology
spellingShingle Stephanie Kourakis
Cara A. Timpani
Ryan M. Bagaric
Bo Qi
Benazir A. Ali
Rebecca Boyer
Guinevere Spiesberger
Nitika Kandhari
Xu Yan
Jujiao Kuang
Ankita Tulangekar
Judy B. de Haan
Deanna Deveson-Lucas
Nicole Stupka
Dirk Fischer
Emma Rybalka
Repurposed Nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of Duchenne muscular dystrophy
Redox Biology
Duchenne muscular dystrophy
Dimethyl fumarate
Therapeutics
Muscle pathology
title Repurposed Nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of Duchenne muscular dystrophy
title_full Repurposed Nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of Duchenne muscular dystrophy
title_fullStr Repurposed Nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of Duchenne muscular dystrophy
title_full_unstemmed Repurposed Nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of Duchenne muscular dystrophy
title_short Repurposed Nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of Duchenne muscular dystrophy
title_sort repurposed nrf2 activator dimethyl fumarate rescues muscle inflammation and fibrosis in an aggravated mdx mouse model of duchenne muscular dystrophy
topic Duchenne muscular dystrophy
Dimethyl fumarate
Therapeutics
Muscle pathology
url http://www.sciencedirect.com/science/article/pii/S2213231725001892
work_keys_str_mv AT stephaniekourakis repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT caraatimpani repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT ryanmbagaric repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT boqi repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT benaziraali repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT rebeccaboyer repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT guineverespiesberger repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT nitikakandhari repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT xuyan repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT jujiaokuang repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT ankitatulangekar repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT judybdehaan repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT deannadevesonlucas repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT nicolestupka repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT dirkfischer repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy
AT emmarybalka repurposednrf2activatordimethylfumaraterescuesmuscleinflammationandfibrosisinanaggravatedmdxmousemodelofduchennemusculardystrophy