Failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of Duchenne muscular dystrophy

Abstract Absence of dystrophin protein causes cardiac dysfunction in patients with Duchenne muscular dystrophy (DMD). Unlike boys with DMD, the common mouse model of DMD (B10-mdx) does not manifest cardiac deficits until late adulthood. This has limited our understanding of the mechanism and therape...

Full description

Saved in:
Bibliographic Details
Main Authors: James S. Novak, Amy Lischin, Prech Uapinyoying, Ravi Hindupur, Young Jae Moon, Surajit Bhattacharya, Sarah Tiufekchiev-Grieco, Victoria Barone, Davi A. G. Mázala, Iteoluwakishi H. Gamu, Gabriela Walters, Jyoti K. Jaiswal
Format: Article
Language:English
Published: Nature Publishing Group 2025-07-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07816-5
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849331634599362560
author James S. Novak
Amy Lischin
Prech Uapinyoying
Ravi Hindupur
Young Jae Moon
Surajit Bhattacharya
Sarah Tiufekchiev-Grieco
Victoria Barone
Davi A. G. Mázala
Iteoluwakishi H. Gamu
Gabriela Walters
Jyoti K. Jaiswal
author_facet James S. Novak
Amy Lischin
Prech Uapinyoying
Ravi Hindupur
Young Jae Moon
Surajit Bhattacharya
Sarah Tiufekchiev-Grieco
Victoria Barone
Davi A. G. Mázala
Iteoluwakishi H. Gamu
Gabriela Walters
Jyoti K. Jaiswal
author_sort James S. Novak
collection DOAJ
description Abstract Absence of dystrophin protein causes cardiac dysfunction in patients with Duchenne muscular dystrophy (DMD). Unlike boys with DMD, the common mouse model of DMD (B10-mdx) does not manifest cardiac deficits until late adulthood. This has limited our understanding of the mechanism and therapeutic approaches to target the pediatric onset of cardiac pathology in DMD. Here we show that the mdx mouse model on the DBA/2 J genetic background (D2-mdx) displays juvenile-onset cardiac degeneration. Molecular and histological analysis revealed that cardiac damage in this model is linked to increased leukocyte chemotactic signaling and an inability to resolve inflammation. These deficiencies result in chronic inflammation and fibrotic conversion of the extracellular matrix (ECM) in the juvenile D2-mdx heart. To address these pathologies, we tested the utility of pro-resolution therapy to clear chronic cardiac inflammation. Use of an N-formyl peptide receptor (FPR) agonist helped physiologically resolve inflammation and mitigate the downstream events that lead to fibrotic degeneration of cardiomyocytes, preventing juvenile onset cardiac muscle loss. These results establish the utility of D2-mdx model to study events associated with pediatric-onset cardiac damage and demonstrates pro-resolution therapy as an alternate to anti-inflammatory therapy for treating degenerative cardiac pathology that leads to cardiomyopathy in DMD.
format Article
id doaj-art-3fe864d6a9844c7eaa689288eb3e09b6
institution Kabale University
issn 2041-4889
language English
publishDate 2025-07-01
publisher Nature Publishing Group
record_format Article
series Cell Death and Disease
spelling doaj-art-3fe864d6a9844c7eaa689288eb3e09b62025-08-20T03:46:28ZengNature Publishing GroupCell Death and Disease2041-48892025-07-0116111110.1038/s41419-025-07816-5Failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of Duchenne muscular dystrophyJames S. Novak0Amy Lischin1Prech Uapinyoying2Ravi Hindupur3Young Jae Moon4Surajit Bhattacharya5Sarah Tiufekchiev-Grieco6Victoria Barone7Davi A. G. Mázala8Iteoluwakishi H. Gamu9Gabriela Walters10Jyoti K. Jaiswal11Center for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalCenter for Genetic Medicine Research, Children’s National Research Institute, Children’s National Research and Innovation Campus, Children’s National HospitalAbstract Absence of dystrophin protein causes cardiac dysfunction in patients with Duchenne muscular dystrophy (DMD). Unlike boys with DMD, the common mouse model of DMD (B10-mdx) does not manifest cardiac deficits until late adulthood. This has limited our understanding of the mechanism and therapeutic approaches to target the pediatric onset of cardiac pathology in DMD. Here we show that the mdx mouse model on the DBA/2 J genetic background (D2-mdx) displays juvenile-onset cardiac degeneration. Molecular and histological analysis revealed that cardiac damage in this model is linked to increased leukocyte chemotactic signaling and an inability to resolve inflammation. These deficiencies result in chronic inflammation and fibrotic conversion of the extracellular matrix (ECM) in the juvenile D2-mdx heart. To address these pathologies, we tested the utility of pro-resolution therapy to clear chronic cardiac inflammation. Use of an N-formyl peptide receptor (FPR) agonist helped physiologically resolve inflammation and mitigate the downstream events that lead to fibrotic degeneration of cardiomyocytes, preventing juvenile onset cardiac muscle loss. These results establish the utility of D2-mdx model to study events associated with pediatric-onset cardiac damage and demonstrates pro-resolution therapy as an alternate to anti-inflammatory therapy for treating degenerative cardiac pathology that leads to cardiomyopathy in DMD.https://doi.org/10.1038/s41419-025-07816-5
spellingShingle James S. Novak
Amy Lischin
Prech Uapinyoying
Ravi Hindupur
Young Jae Moon
Surajit Bhattacharya
Sarah Tiufekchiev-Grieco
Victoria Barone
Davi A. G. Mázala
Iteoluwakishi H. Gamu
Gabriela Walters
Jyoti K. Jaiswal
Failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of Duchenne muscular dystrophy
Cell Death and Disease
title Failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of Duchenne muscular dystrophy
title_full Failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of Duchenne muscular dystrophy
title_fullStr Failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of Duchenne muscular dystrophy
title_full_unstemmed Failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of Duchenne muscular dystrophy
title_short Failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of Duchenne muscular dystrophy
title_sort failure to resolve inflammation contributes to juvenile onset cardiac damage in a mouse model of duchenne muscular dystrophy
url https://doi.org/10.1038/s41419-025-07816-5
work_keys_str_mv AT jamessnovak failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT amylischin failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT prechuapinyoying failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT ravihindupur failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT youngjaemoon failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT surajitbhattacharya failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT sarahtiufekchievgrieco failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT victoriabarone failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT daviagmazala failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT iteoluwakishihgamu failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT gabrielawalters failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy
AT jyotikjaiswal failuretoresolveinflammationcontributestojuvenileonsetcardiacdamageinamousemodelofduchennemusculardystrophy