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      Interleukin-1beta (IL-1β)-induced Notch ligand Jagged1 suppresses mitogenic action of IL-1β on human dystrophic myogenic cells

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          Abstract

          Duchenne muscular dystrophy (DMD) is a severe X-linked recessive muscle disorder caused by mutations in the dystrophin gene. Nonetheless, secondary processes involving perturbation of muscle regeneration probably exacerbate disease progression, resulting in the fatal loss of muscle in DMD patients. A dysfunction of undifferentiated myogenic cells is the most likely cause for the reduction of regenerative capacity of muscle. To clarify molecular mechanisms in perturbation of the regenerative capacity of DMD muscle, we have established several NCAM (CD56)-positive immortalized human dystrophic and non-dystrophic myogenic cell lines from DMD and healthy muscles. A pro-inflammatory cytokine, IL-1β, promoted cell cycle progression of non-dystrophic myogenic cells but not DMD myogenic cells. In contrast, IL-1β upregulated the Notch ligand Jagged1 gene in DMD myogenic cells but not in non-dystrophic myogenic cells. Knockdown of Jagged1 in DMD myogenic cells restored the IL-1β-promoted cell cycle progression. Conversely, enforced expression of Jagged1-blocked IL-1β promoted proliferation of non-dystrophic myogenic cells. In addition, IL-1β prevented myogenic differentiation of DMD myogenic cells depending on Jagged1 but not of non-dystrophic myogenic cells. These results demonstrate that Jagged1 induced by IL-1β in DMD myogenic cells modified the action of IL-1β and reduced the ability to proliferate and differentiate. IL-1β induced Jagged1 gene expression may be a feedback response to excess stimulation with this cytokine because high IL-1β (200–1000 pg/ml) induced Jagged1 gene expression even in non-dystrophic myogenic cells. DMD myogenic cells are likely to acquire the susceptibility of the Jagged1 gene to IL-1β under the microcircumstances in DMD muscles. The present results suggest that Jagged1 induced by IL-1β plays a crucial role in the loss of muscle regeneration capacity of DMD muscles. The IL-1β/Jagged1 pathway may be a new therapeutic target to ameliorate exacerbation of muscular dystrophy in a dystrophin-independent manner.

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          Most cited references38

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          Regulatory interactions between muscle and the immune system during muscle regeneration.

          Recent discoveries reveal complex interactions between skeletal muscle and the immune system that regulate muscle regeneration. In this review, we evaluate evidence that indicates that the response of myeloid cells to muscle injury promotes muscle regeneration and growth. Acute perturbations of muscle activate a sequence of interactions between muscle and inflammatory cells. The initial inflammatory response is a characteristic Th1 inflammatory response, first dominated by neutrophils and subsequently by CD68(+) M1 macrophages. M1 macrophages can propagate the Th1 response by releasing proinflammatory cytokines and cause further tissue damage through the release of nitric oxide. Myeloid cells in the early Th1 response stimulate the proliferative phase of myogenesis through mechanisms mediated by TNF-alpha and IL-6; experimental prolongation of their presence is associated with delayed transition to the early differentiation stage of myogenesis. Subsequent invasion by CD163(+)/CD206(+) M2 macrophages attenuates M1 populations through the release of anti-inflammatory cytokines, including IL-10. M2 macrophages play a major role in promoting growth and regeneration; their absence greatly slows muscle growth following injury or modified use and inhibits muscle differentiation and regeneration. Chronic muscle injury leads to profiles of macrophage invasion and function that differ from acute injuries. For example, mdx muscular dystrophy yields invasion of muscle by M1 macrophages, but their early invasion is accompanied by a subpopulation of M2a macrophages. M2a macrophages are IL-4 receptor(+)/CD206(+) cells that reduce cytotoxicity of M1 macrophages. Subsequent invasion of dystrophic muscle by M2c macrophages is associated with progression of the regenerative phase in pathophysiology. Together, these findings show that transitions in macrophage phenotype are an essential component of muscle regeneration in vivo following acute or chronic muscle damage.
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            Notch-mediated restoration of regenerative potential to aged muscle.

            A hallmark of aging is diminished regenerative potential of tissues, but the mechanism of this decline is unknown. Analysis of injured muscle revealed that, with age, resident precursor cells (satellite cells) had a markedly impaired propensity to proliferate and to produce myoblasts necessary for muscle regeneration. This was due to insufficient up-regulation of the Notch ligand Delta and, thus, diminished activation of Notch in aged, regenerating muscle. Inhibition of Notch impaired regeneration of young muscle, whereas forced activation of Notch restored regenerative potential to old muscle. Thus, Notch signaling is a key determinant of muscle regenerative potential that declines with age.
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              NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia.

              MyoD regulates skeletal muscle differentiation (SMD) and is essential for repair of damaged tissue. The transcription factor nuclear factor kappa B (NF-kappaB) is activated by the cytokine tumor necrosis factor (TNF), a mediator of skeletal muscle wasting in cachexia. Here, the role of NF-kappaB in cytokine-induced muscle degeneration was explored. In differentiating C2C12 myocytes, TNF-induced activation of NF-kappaB inhibited SMD by suppressing MyoD mRNA at the posttranscriptional level. In contrast, in differentiated myotubes, TNF plus interferon-gamma (IFN-gamma) signaling was required for NF-kappaB-dependent down-regulation of MyoD and dysfunction of skeletal myofibers. MyoD mRNA was also down-regulated by TNF and IFN-gamma expression in mouse muscle in vivo. These data elucidate a possible mechanism that may underlie the skeletal muscle decay in cachexia.
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                Author and article information

                Contributors
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 December 2017
                2017
                : 12
                : 12
                : e0188821
                Affiliations
                [1 ] Department of Regenerative Medicine, National Center for Geriatrics and Gerontology, Morioka, Oobu, Aichi, Japan
                [2 ] Division of Carcinogenesis and Cancer Prevention, National Cancer Center Research Institute, Tsukiji, Chuo-ku, Tokyo, Japan
                [3 ] Department of Urology, National Center for Geriatrics and Gerontology, Morioka, Oobu, Aichi, Japan
                [4 ] Department of Mental Retardation and Birth Defect Research, National Institute of Neuroscience, Nervous, and Muscular Disorders, National Center of Neurology and Psychiatry,Ogawahigashi, Kodaira, Tokyo, Japan
                [5 ] Department of Medical Rehabilitation, Faculty of Rehabilitation, Kobegakuin University, Ikawadani-cho, Nishi-ku, Kobe Japan
                University of Minnesota Medical Center, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                [¤a]

                Current address: Department of Clinical Research, Higashinagoya National Hospital, Meito-ku, Nagoya, Aichi, Japan.

                [¤b]

                Current address: Gerontology of Motor Systems, Research Team for Geriatric Medicine, Tokyo Metropolitan Geriatric Hospital and Institute of Gerontology, Itabashi-ku, Tokyo, Japan

                Author information
                http://orcid.org/0000-0002-9231-8053
                Article
                PONE-D-17-35609
                10.1371/journal.pone.0188821
                5711031
                29194448
                b916cca8-3b42-4872-9137-24f6895a40f3
                © 2017 Nagata et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 3 October 2017
                : 14 November 2017
                Page count
                Figures: 10, Tables: 0, Pages: 23
                Funding
                Funded by: The Research Funding for Longevity Sciences from National Center for Geriatrics and Gerontology (NCGG), Japan
                Award ID: (28-24, 28-39)
                Award Recipient :
                Funded by: Intramural Research Grant for Neurological and Psychiatric Disorders of NCNP, Japan
                Award ID: (25-5, 28-6)
                Award Recipient :
                Funded by: Grants-in-Aid for Scientific Research Japan
                Award ID: (KAKENHI,15K10426)
                Award Recipient :
                This work was supported by Grants-in-Aid for Scientific Research (KAKENHI,15K10426), Japan, Intramural Research Grant (25-5, 28-6) for Neurological and Psychiatric Disorders of NCNP, Japan, and The Research Funding for Longevity Sciences (28-24, 28-39) from National Center for Geriatrics and Gerontology (NCGG), Japan.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Morphogenesis
                Muscle Differentiation
                Biology and Life Sciences
                Developmental Biology
                Morphogenesis
                Regeneration
                Muscle Regeneration
                Biology and Life Sciences
                Developmental Biology
                Organism Development
                Regeneration
                Muscle Regeneration
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Cell Biology
                Cell Physiology
                Cell Immortalization
                Medicine and Health Sciences
                Neurology
                Muscular Dystrophies
                Duchenne Muscular Dystrophy
                Medicine and Health Sciences
                Clinical Genetics
                X-Linked Traits
                Duchenne Muscular Dystrophy
                Biology and Life Sciences
                Genetics
                Heredity
                Genetic Linkage
                Sex Linkage
                X-Linked Traits
                Duchenne Muscular Dystrophy
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Skeletal Muscles
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Skeletal Muscles
                Research and Analysis Methods
                Spectrum Analysis Techniques
                Spectrophotometry
                Cytophotometry
                Flow Cytometry
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Muscle Cells
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Muscle Tissue
                Muscle Cells
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Muscle Tissue
                Muscle Cells
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                All relevant data are within the paper and its Supporting Information files.

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