Cited by 512Muscle Physiology and DisordersImmune cells in cancerNeurogenetic and Muscular Disorders Research

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Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy

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Villalta, S. A., Nguyen, H. X., Deng, B., Gotoh, T., Tidball, J. G.·2008·Human Molecular Genetics

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Abstract

Duchenne muscular dystrophy (DMD) is the most common, lethal, muscle-wasting disease of childhood. Previous investigations have shown that muscle macrophages may play an important role in promoting the pathology in the mdx mouse model of DMD. In the present study, we investigate the mechanism through which macrophages promote mdx dystrophy and assess whether the phenotype of the macrophages changes between the stage of peak muscle necrosis (4 weeks of age) and muscle regeneration (12 weeks). We find that 4-week-old mdx muscles contain a population of pro-inflammatory, classically activated M1 macrophages that lyse muscle in vitro by NO-mediated mechanisms. Genetic ablation of the iNOS gene in mdx mice also significantly reduces muscle membrane lysis in 4-week-old mdx mice in vivo. However, 4-week mdx muscles also contain a population of alternatively activated, M2a macrophages that express arginase. In vitro assays show that M2a macrophages reduce lysis of muscle cells by M1 macrophages through the competition of arginase in M2a cells with iNOS in M1 cells for their common, enzymatic substrate, arginine. During the transition from the acute peak of mdx pathology to the regenerative stage, expression of IL-4 and IL-10 increases, either of which can deactivate the M1 phenotype and promote activation of a CD163+, M2c phenotype that can increase tissue repair. Our findings further show that IL-10 stimulation of macrophages activates their ability to promote satellite cell proliferation. Deactivation of the M1 phenotype is also associated with a reduced expression of iNOS, IL-6, MCP-1 and IP-10. Thus, these results show that distinct subpopulations of macrophages can promote muscle injury or repair in muscular dystrophy, and that therapeutic interventions that affect the balance between M1 and M2 macrophage populations may influence the course of muscular dystrophy.

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Authors: Villalta, S. A., Nguyen, H. X., Deng, B., Gotoh, T., & Tidball, J. G.
Affiliations: University of California, Los Angeles (US)
Kumamoto University (JP)
Corresponding author: Tidball, J. G.
ORCID: Villalta, S. A.
Deng, B.
Gotoh, T.
Tidball, J. G.
Venue: Human Molecular Genetics
Publisher: Oxford University Press (OUP)
Published: 2008-11-07
Volume: 18
Issue: 3
Pages: 482-496
ISSN: 0964-6906 (ISSN-L)
1460-2083
DOI: 10.1093/hmg/ddn376
PMC: PMC2638796
OpenAlex: W2144067550
Cited by: 512
References: 60
Citations by year: 2026: 11 · 2025: 25 · 2024: 18 · 2023: 28 · 2022: 41 · 2021: 32 · 2020: 32 · 2019: 33 · 2018: 39 · 2017: 37 · 2016: 25 · 2015: 39 · 2014: 40 · 2013: 32 · 2012: 27
FWCI: 7.14
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Human Molecular Genetics (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HighWire Press Open Archive (submittedVersion)
Funders: Muscular Dystrophy Association
National Institutes of Health (5r01ar040343-12, AR40343)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR047855, R01 AR47721, R01 AR 40343, R01AR047721, F31AR054724)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Health Sciences › Medicine › Genetics (clinical) › Neurogenetic and Muscular Disorders Research
Keywords: Duchenne muscular dystrophy, mdx mice, macrophage polarization, M1 macrophages, M2 macrophages, arginine metabolism, arginase, inducible nitric oxide synthase, nitric oxide, muscle necrosis, muscle regeneration, IL-10, IL-4, CD163, satellite cell proliferation, tissue repair
MeSH terms: Animals, Arginine, Cells, Cultured, Humans, Macrophage Activation, Macrophages, Mice, Inbred C57BL, Mice, Transgenic, Muscular Dystrophy, Animal, Nitric Oxide, Phenotype, Severity of Illness Index, Cytokines, Muscle, Skeletal, Muscular Dystrophy, Duchenne, Cell Proliferation, Mice, Nitric Oxide Synthase Type II

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Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy

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