Microbiota dysbiosis influences immune system and muscle pathophysiology of dystrophin‐deficient mice
Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in DMD , encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gu...
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| Published in | EMBO molecular medicine Vol. 15; no. 3; pp. e16244 - n/a |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
08.03.2023
EMBO Press John Wiley and Sons Inc Springer Nature |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in
DMD
, encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of
Prevotella
. Furthermore, the absence of gut microbes through the generation of mdx germ‐free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD.
Synopsis
The susceptibility of DMD patients to inflammatory events cannot solely be explained by skeletal muscle genetic defects but rather favors a new paradigm linking development of chronic inflammation with a strict regulation between epigenetics factors and degenerative environment.
Gut microbiota–specific alterations (dysbiosis) correlate with the dystrophic pathology in mdx mice, influencing muscle immunity and fibrosis.
Dysbiotic mdx microbiota induces a decreased innate immune response and altered muscle metabolism.
The study of the dysregulated immune system‐microbiota axis in mdx mice highlights the importance of microbiota as a potential target for therapeutic interventions.
Graphical Abstract
The susceptibility of DMD patients to inflammatory events cannot solely be explained by skeletal muscle genetic defects but rather favors a new paradigm linking the development of chronic inflammation with a strict regulation between epigenetics factors and degenerative environment. |
|---|---|
| AbstractList | Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in
DMD
, encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of
Prevotella
. Furthermore, the absence of gut microbes through the generation of mdx germ‐free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD.
Synopsis
The susceptibility of DMD patients to inflammatory events cannot solely be explained by skeletal muscle genetic defects but rather favors a new paradigm linking development of chronic inflammation with a strict regulation between epigenetics factors and degenerative environment.
Gut microbiota–specific alterations (dysbiosis) correlate with the dystrophic pathology in mdx mice, influencing muscle immunity and fibrosis.
Dysbiotic mdx microbiota induces a decreased innate immune response and altered muscle metabolism.
The study of the dysregulated immune system‐microbiota axis in mdx mice highlights the importance of microbiota as a potential target for therapeutic interventions.
Graphical Abstract
The susceptibility of DMD patients to inflammatory events cannot solely be explained by skeletal muscle genetic defects but rather favors a new paradigm linking the development of chronic inflammation with a strict regulation between epigenetics factors and degenerative environment. Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in DMD , encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of Prevotella . Furthermore, the absence of gut microbes through the generation of mdx germ‐free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD. image The susceptibility of DMD patients to inflammatory events cannot solely be explained by skeletal muscle genetic defects but rather favors a new paradigm linking development of chronic inflammation with a strict regulation between epigenetics factors and degenerative environment. Gut microbiota–specific alterations (dysbiosis) correlate with the dystrophic pathology in mdx mice, influencing muscle immunity and fibrosis. Dysbiotic mdx microbiota induces a decreased innate immune response and altered muscle metabolism. The study of the dysregulated immune system‐microbiota axis in mdx mice highlights the importance of microbiota as a potential target for therapeutic interventions. Duchenne muscular dystrophy (DMD) is a progressive severe muscle-wasting disease caused by mutations in DMD, encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of Prevotella. Furthermore, the absence of gut microbes through the generation of mdx germ-free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD. Abstract Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in DMD, encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of Prevotella. Furthermore, the absence of gut microbes through the generation of mdx germ‐free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD. Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in DMD , encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of Prevotella . Furthermore, the absence of gut microbes through the generation of mdx germ‐free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD. The susceptibility of DMD patients to inflammatory events cannot solely be explained by skeletal muscle genetic defects but rather favors a new paradigm linking the development of chronic inflammation with a strict regulation between epigenetics factors and degenerative environment. Duchenne muscular dystrophy (DMD) is a progressive severe muscle-wasting disease caused by mutations in DMD, encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of Prevotella. Furthermore, the absence of gut microbes through the generation of mdx germ-free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD.Duchenne muscular dystrophy (DMD) is a progressive severe muscle-wasting disease caused by mutations in DMD, encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of Prevotella. Furthermore, the absence of gut microbes through the generation of mdx germ-free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD. Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in DMD, encoding dystrophin, that leads to loss of muscle function with cardiac/respiratory failure and premature death. Since dystrophic muscles are sensed by infiltrating inflammatory cells and gut microbial communities can cause immune dysregulation and metabolic syndrome, we sought to investigate whether intestinal bacteria support the muscle immune response in mdx dystrophic murine model. We highlighted a strong correlation between DMD disease features and the relative abundance of Prevotella. Furthermore, the absence of gut microbes through the generation of mdx germ‐free animal model, as well as modulation of the microbial community structure by antibiotic treatment, influenced muscle immunity and fibrosis. Intestinal colonization of mdx mice with eubiotic microbiota was sufficient to reduce inflammation and improve muscle pathology and function. This work identifies a potential role for the gut microbiota in the pathogenesis of DMD. Synopsis The susceptibility of DMD patients to inflammatory events cannot solely be explained by skeletal muscle genetic defects but rather favors a new paradigm linking development of chronic inflammation with a strict regulation between epigenetics factors and degenerative environment. Gut microbiota–specific alterations (dysbiosis) correlate with the dystrophic pathology in mdx mice, influencing muscle immunity and fibrosis. Dysbiotic mdx microbiota induces a decreased innate immune response and altered muscle metabolism. The study of the dysregulated immune system‐microbiota axis in mdx mice highlights the importance of microbiota as a potential target for therapeutic interventions. The susceptibility of DMD patients to inflammatory events cannot solely be explained by skeletal muscle genetic defects but rather favors a new paradigm linking the development of chronic inflammation with a strict regulation between epigenetics factors and degenerative environment. |
| Author | Tripodi, Luana Lonati, Caterina Baselli, Guido Facoetti, Amanda Caprioli, Flavio Troisi, Jacopo Villa, Chiara Landolfi, Annamaria Quattrocelli, Mattia Farini, Andrea Wintzinger, Michelle Cassani, Barbara Molinaro, Davide Strati, Francesco Facciotti, Federica Torrente, Yvan Gatti, Stefano |
| AuthorAffiliation | 6 Translational Medicine – Department of Transfusion Medicine and Hematology Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico Milan Italy 12 Department of Medical Biotechnologies and Translational Medicine Università Degli Studi di Milano Milan Italy 1 Neurology Unit Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico Milan Italy 3 Mucosal Immunology Lab, Department of Experimental Oncology IEO‐European Institute of Oncology Milan Italy 8 Theoreo Srl, Spinoff Company of the University of Salerno Montecorvino Pugliano Italy 10 Molecular Cardiovascular Biology Division, Heart Institute Cincinnati Children's Hospital Medical Center Cincinnati OH USA 5 Humanitas Clinical and Research Center IRCCS Milan Italy 9 Center for Surgical Research Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico Milan Italy 13 Unit of Gastroenterology and Endoscopy, Department of Pathophysiology and Transplantation Università degli Studi di Milano, Fondazione IRCCS Ca' Granda, Ospedale Policlinico |
| AuthorAffiliation_xml | – name: 12 Department of Medical Biotechnologies and Translational Medicine Università Degli Studi di Milano Milan Italy – name: 8 Theoreo Srl, Spinoff Company of the University of Salerno Montecorvino Pugliano Italy – name: 14 Present address: SciLifeLab, Department of Microbiology, Tumor and Cell Biology Karolinska Institutet Solna Sweden – name: 4 Humanitas University Milan Italy – name: 1 Neurology Unit Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico Milan Italy – name: 13 Unit of Gastroenterology and Endoscopy, Department of Pathophysiology and Transplantation Università degli Studi di Milano, Fondazione IRCCS Ca' Granda, Ospedale Policlinico di Milano Milan Italy – name: 9 Center for Surgical Research Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico Milan Italy – name: 3 Mucosal Immunology Lab, Department of Experimental Oncology IEO‐European Institute of Oncology Milan Italy – name: 5 Humanitas Clinical and Research Center IRCCS Milan Italy – name: 7 Department of Medicine, Surgery and Dentistry, Scuola Medica Salernitana University of Salerno Baronissi Italy – name: 6 Translational Medicine – Department of Transfusion Medicine and Hematology Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico Milan Italy – name: 10 Molecular Cardiovascular Biology Division, Heart Institute Cincinnati Children's Hospital Medical Center Cincinnati OH USA – name: 11 Department of Pediatrics University of Cincinnati College of Medicine Cincinnati OH USA – name: 2 Stem Cell Laboratory, Department of Pathophysiology and Transplantation, Dino Ferrari Center University of Milan Milan Italy |
| Author_xml | – sequence: 1 givenname: Andrea surname: Farini fullname: Farini, Andrea organization: Neurology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico – sequence: 2 givenname: Luana orcidid: 0000-0003-4446-2840 surname: Tripodi fullname: Tripodi, Luana organization: Stem Cell Laboratory, Department of Pathophysiology and Transplantation, Dino Ferrari Center, University of Milan – sequence: 3 givenname: Chiara surname: Villa fullname: Villa, Chiara organization: Stem Cell Laboratory, Department of Pathophysiology and Transplantation, Dino Ferrari Center, University of Milan – sequence: 4 givenname: Francesco orcidid: 0000-0001-7217-3355 surname: Strati fullname: Strati, Francesco organization: Mucosal Immunology Lab, Department of Experimental Oncology, IEO‐European Institute of Oncology – sequence: 5 givenname: Amanda surname: Facoetti fullname: Facoetti, Amanda organization: Humanitas University, Humanitas Clinical and Research Center IRCCS – sequence: 6 givenname: Guido surname: Baselli fullname: Baselli, Guido organization: Translational Medicine – Department of Transfusion Medicine and Hematology, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, SciLifeLab, Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet – sequence: 7 givenname: Jacopo orcidid: 0000-0003-2962-7379 surname: Troisi fullname: Troisi, Jacopo organization: Department of Medicine, Surgery and Dentistry, Scuola Medica Salernitana, University of Salerno, Theoreo Srl, Spinoff Company of the University of Salerno – sequence: 8 givenname: Annamaria surname: Landolfi fullname: Landolfi, Annamaria organization: Department of Medicine, Surgery and Dentistry, Scuola Medica Salernitana, University of Salerno, Theoreo Srl, Spinoff Company of the University of Salerno – sequence: 9 givenname: Caterina surname: Lonati fullname: Lonati, Caterina organization: Center for Surgical Research, Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico – sequence: 10 givenname: Davide orcidid: 0000-0001-7536-208X surname: Molinaro fullname: Molinaro, Davide organization: Neurology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Stem Cell Laboratory, Department of Pathophysiology and Transplantation, Dino Ferrari Center, University of Milan – sequence: 11 givenname: Michelle surname: Wintzinger fullname: Wintzinger, Michelle organization: Molecular Cardiovascular Biology Division, Heart Institute, Cincinnati Children's Hospital Medical Center, Department of Pediatrics, University of Cincinnati College of Medicine – sequence: 12 givenname: Stefano orcidid: 0000-0003-2209-4338 surname: Gatti fullname: Gatti, Stefano organization: Center for Surgical Research, Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico – sequence: 13 givenname: Barbara surname: Cassani fullname: Cassani, Barbara organization: Humanitas Clinical and Research Center IRCCS, Department of Medical Biotechnologies and Translational Medicine, Università Degli Studi di Milano – sequence: 14 givenname: Flavio surname: Caprioli fullname: Caprioli, Flavio organization: Unit of Gastroenterology and Endoscopy, Department of Pathophysiology and Transplantation, Università degli Studi di Milano, Fondazione IRCCS Ca' Granda, Ospedale Policlinico di Milano – sequence: 15 givenname: Federica surname: Facciotti fullname: Facciotti, Federica organization: Unit of Gastroenterology and Endoscopy, Department of Pathophysiology and Transplantation, Università degli Studi di Milano, Fondazione IRCCS Ca' Granda, Ospedale Policlinico di Milano – sequence: 16 givenname: Mattia surname: Quattrocelli fullname: Quattrocelli, Mattia organization: Molecular Cardiovascular Biology Division, Heart Institute, Cincinnati Children's Hospital Medical Center, Department of Pediatrics, University of Cincinnati College of Medicine – sequence: 17 givenname: Yvan orcidid: 0000-0002-2705-3984 surname: Torrente fullname: Torrente, Yvan email: yvan.torrente@unimi.it organization: Neurology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Stem Cell Laboratory, Department of Pathophysiology and Transplantation, Dino Ferrari Center, University of Milan |
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| Keywords | T‐lymphocytes immunity Duchenne muscular dystrophy gut microbiota skeletal muscle metabolism T-lymphocytes |
| Language | English |
| License | Attribution 2022 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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| Notes | See also March 2023 A Jayaraman & S Pettersson ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 See also: A Jayaraman & S Pettersson (March 2023) |
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| PublicationTitle | EMBO molecular medicine |
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| Snippet | Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in
DMD
, encoding dystrophin, that leads to loss of muscle... Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in DMD, encoding dystrophin, that leads to loss of muscle... Duchenne muscular dystrophy (DMD) is a progressive severe muscle-wasting disease caused by mutations in DMD, encoding dystrophin, that leads to loss of muscle... Abstract Duchenne muscular dystrophy (DMD) is a progressive severe muscle‐wasting disease caused by mutations in DMD, encoding dystrophin, that leads to loss... |
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| StartPage | e16244 |
| SubjectTerms | Animal models Animals Antibiotics Cardiac muscle Community structure Digestive system Disease Disease Models, Animal Duchenne muscular dystrophy Duchenne's muscular dystrophy Dysbacteriosis Dysbiosis Dystrophin Dystrophin - genetics EMBO12 EMBO23 EMBO25 Fibrosis Functional foods & nutraceuticals Gastrointestinal tract Genotype & phenotype Germfree gut microbiota Homeostasis Immune response Immune system Immune System - metabolism Immune System - pathology immunity Inflammation Intestinal microflora Intestine Lymphocytes Metabolic syndrome Metabolism Metabolites Mice Mice, Inbred mdx Microbiota Microorganisms Motility Muscle function Muscle, Skeletal - metabolism Muscular dystrophy Muscular Dystrophy, Duchenne - genetics Musculoskeletal system Nitric oxide Pathophysiology Respiratory failure skeletal muscle metabolism Smooth muscle T‐lymphocytes |
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| Title | Microbiota dysbiosis influences immune system and muscle pathophysiology of dystrophin‐deficient mice |
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