Cited by 854Muscle Physiology and DisordersCardiac Fibrosis and RemodelingWound Healing and Treatments

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Aberrant repair and fibrosis development in skeletal muscle

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Mann, Christopher J, Perdiguero, Eusebio, Kharraz, Yacine, Aguilar, Susana, Pessina, Patrizia, Serrano, Antonio L, Muñoz-Cánoves, Pura·2011·Skeletal Muscle

DOI 10.1186/2044-5040-1-21PMC PMC3156644

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Abstract

The repair process of damaged tissue involves the coordinated activities of several cell types in response to local and systemic signals. Following acute tissue injury, infiltrating inflammatory cells and resident stem cells orchestrate their activities to restore tissue homeostasis. However, during chronic tissue damage, such as in muscular dystrophies, the inflammatory-cell infiltration and fibroblast activation persists, while the reparative capacity of stem cells (satellite cells) is attenuated. Abnormal dystrophic muscle repair and its end stage, fibrosis, represent the final common pathway of virtually all chronic neurodegenerative muscular diseases. As our understanding of the pathogenesis of muscle fibrosis has progressed, it has become evident that the muscle provides a useful model for the regulation of tissue repair by the local microenvironment, showing interplay among muscle-specific stem cells, inflammatory cells, fibroblasts and extracellular matrix components of the mammalian wound-healing response. This article reviews the emerging findings of the mechanisms that underlie normal versus aberrant muscle-tissue repair.

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Figure 1 Extracellular matrix (ECM) deposition in acute and chronic muscle regeneration. Acute injury to healthy muscle produces rapid and controlled inflammation that removes dead and damaged myofibers, and promotes replacement of the injured muscle. However, in conditions of chronic injury, as occurs in the muscular dystrophies, chronic inflammatory events result in the excessive accumulation of ECM components, which inhibit myogenic repair and lead to muscle being replaced by fibrotic/scar tissue. (Top) Tibialis anterior muscles of mice were injected with cardiotoxin and samples were taken at different stages of the regeneration process. A representative sample showing the inflammatory phase, characterized by a transient increase in collagen deposition, and subsequently the resolving phase of healing, with progressive recovery of the normal tissue morphology (hematoxylin and eosin). (Bottom) Evolution of the morphological changes seen in the diaphragm of mdx dystrophic mice with disease progression, leading to heterogeneity in fiber size and increased collagen deposition between the altered myofibers. Bars = 50 μm.CC BY · PubMed Central

Figure 2 Chronic inflammation leads to fibrosis in skeletal-muscle repair. Resident and extravasating peripheral macrophages play an important role in the early stages of muscle repair after acute injury, with pro-inflammatory (M1) macrophages first acting to clear the damage, and anti-inflammatory (M2c) macrophages and alternatively activated macrophages (M2a), implicated in the subsequent resumption of inflammation, extracellular matrix (ECM) deposition and tissue repair. M2c and M2a macrophages release anti-inflammatory cytokines and pro-fibrotic molecules such as transforming growth factor (TGF)-β, which in turn activate fibroblasts in a regulated manner to produce ECM components and ECM-remodeling factors, including autocrine production of TGFβ, collagen, fibronectin, serine proteases (such as uPA/plasmin), and metalloproteinases (MMPs) and their inhibitors (TIMPs). However, during chronic tissue damage, as in muscular dystrophies, the increased and persistent presence of macrophages modify the intensity, duration and interactions of these released factors, leading to excessive ECM accumulation and replacement of muscle with fibrotic tissue.CC BY · PubMed Central

Figure 3 Inflammatory control of skeletal-muscle regeneration. Replacement of damaged muscle fibers is dependent on satellite cells, resident stem cells that are normally quiescent, and are located under the basal lamina of muscle fibers. Tissue damage leads to their activation, proliferation, differentiation and fusion to form new myofibers. However, their capacity to mediate repair is modified by the extent and type of injury, and consequently by their interaction with various cellular and soluble mediators, most importantly with infiltrating macrophages. The proposed paracrine interaction between macrophages and satellite cells is as follows. During the timely, regulated process of regeneration after acute injury (left), pro-inflammatory cytokines released from M1-macrophages may promote satellite-cell proliferation, whereas cytokines released by anti-inflammatory (M2c) and alternatively activated (M2a) macrophages, respectively, may favor their differentiation and fusion. In particular, interleukin (IL)-4 was shown to regulate fusion of myoblasts in vitro and in vivo [129]. It could be expected that, during chronic damage (right), such as in muscular dystrophies, the increased and persistent presence of the distinct macrophage cell types could modify the relative levels and kinetics of these cytokines, resulting in altered satellite-cell functions and aberrant regeneration, with progressive development of fibrosis and fat accumulation, ultimately leading to non-functional muscle tissue.CC BY · PubMed Central

Figure 4 Inflammatory and fibrotic traits in dystrophic muscle of patients with DMD and mdx mice. (A) Fibrin(ogen) accumulates in muscles of patients with DMD and in aged mdx mice. Immunohistochemistry for fibrin(ogen) (brown) in muscle biopsies of (top) patients with DMD and healthy subjects and in (bottom) wild-type (WT) and mdx diaphragms. (B) Increased fibrosis, fibroblast number and TGFβ signaling in dystrophic muscles. Staining for collagen deposition (Sirius red) and immunohistochemistry for fibroblast-specific protein (FSP)-1 and P-Smad2 was performed on muscle biopsies taken from patients with DMD and healthy subjects. (C) Presence of alternatively activated macrophages in diaphragm muscle of mdx mice. Cells double-positive for CD206 (red) and Arginase I (green) in mdx diaphragm are shown by immunofluorescence with specific antibodies. The relative increase in the number of these cells in the mdx diaphragm over time is shown. Bars = 50 μm.CC BY · PubMed Central

Figure 5 Myofiber growth and extracellular matrix (ECM) accumulation after damage differ in young and aged muscles. (Top) In young muscles in response to injury, the satellite cells under the basal lamina can be activated by environmental cues released by the neighboring cells (a local milieu composed of fibroblasts, interstitial cells, resident macrophages, fibro/adipogenic progenitors (FAPs) and microvasculature-associated cells) to eventually form new fibers almost indistinguishable to the pre-existing ones. (Bottom) In aged muscles, the repair process will result in reduced size of newly formed myofibers and thickening of the basal lamina by enhanced deposition of ECM components, which could potentially be ascribed to the increased presence and activity of resident fibroblasts (and/or FAPs), and to decreased satellite-cell myogenic potential. Conversion of myogenic into fibrogenic cells could also contribute to ECM accumulation. These new microenvironment conditions within the satellite-cell niche will impede efficient satellite-cell functions and muscle repair.CC BY · PubMed Central

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RETRACTED ARTICLE: The role of nitric oxide during healing of trauma to the skeletal muscle
Filippin, L. I., Cuevas, M. J., Lima‐Cabello, E., Marroni, N. P., González‐Gallego, J., & Xavier, R. M. (2010) · Inflammation Research · doi:10.1007/s00011-010-0277-2 · Cited by 34 · cited 4×
“In addition, NO, which is released by local and invading cells during injury, can act as a pro-inflammatory molecule, and is able to activate MMP-2, which in turn releases HGF. Importantly, blockers of NOS function, such as nitro- Larginine methyl ester (L-NAME), have been shown to decrease the acute inflammatory reac…”
MethodInfluential
Retracted
The chemokine system in diverse forms of macrophage activation and polarization
MANTOVANI, A., SICA, A., SOZZANI, S., ALLAVENA, P., VECCHI, A., & LOCATI, M. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.09.015 · Cited by 6,534 · cited 2×
“A nomenclature for polarized macrophages has been proposed [24,25] and they are now referred to as classically and alternatively activated macrophages, or M1 and M2 macrophages, respectively (Figure 2, Figure 3).”
Background
Mechanisms of TGF-β Signaling from Cell Membrane to the Nucleus
Shi, Y., & Massagué, J. (2003) · Cell · doi:10.1016/s0092-8674(03)00432-x · Cited by 5,860
Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases: Structure, Function, and Biochemistry
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Cellular and molecular mechanisms of fibrosis
Wynn, T. (2008) · The Journal of Pathology · doi:10.1002/path.2277 · Cited by 4,495
SATELLITE CELL OF SKELETAL MUSCLE FIBERS
Mauro, A. (1961) · The Journal of Cell Biology · doi:10.1083/jcb.9.2.493 · Cited by 3,683
The Myofibroblast
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“These cells are associated with tissue repair and fibrosis in many tissues and organs, including muscle, skin, liver, lung, bone and cartilage [56].”
Background
Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis
Arnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R. K., & Chazaud, B. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070075 · Cited by 2,002 · cited 3×
“An important development in our understanding of muscle repair and fibrosis was the demonstration that a heterogeneous population of macrophages exists in regenerating muscle after injury, exhibiting opposing activities (either pro-inflammatory or anti-inflammatory) and different kinetics [23].”
BackgroundInfluential
Fibrotic disease and the TH1/TH2 paradigm
Wynn, T. A. (2004) · Nature Reviews Immunology · doi:10.1038/nri1412 · Cited by 1,765
Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis
Joe, A. W. B., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M. A., & Rossi, F. M. V. (2010) · Nature Cell Biology · doi:10.1038/ncb2015 · Cited by 1,690 · cited 7×
“Whether FAP conversion also occurs during aging, and whether Basal lamina ECM deposition Satellite cell Fibro/adipogenic progenitor Resident macrophage Fibroblast Increased number of fibroblasts Fibrogenic-converted myogenic cells Myofiber Atrophic myofiber Young Old Figure 5 Myofiber growth and extracellular matrix (…”
BackgroundInfluential

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“tissue are thought to cause muscle weakness [4,5].”
Background
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T1ρ imaging as a non‐invasive assessment of collagen remodelling and organization in human skeletal muscle after ligamentous injury
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Extracellular vesicle-derived miRNAs improve stem cell-based therapeutic approaches in muscle wasting conditions
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Evaluation of bone marrow mononuclear cells as an adjunct therapy to minced muscle graft for the treatment of volumetric muscle loss injuries
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Authors: Mann, C. J., Perdiguero, E., Kharraz, Y., Aguilar, S., Pessina, P., Serrano, A. L., & Muñoz-Cánoves, P.
Affiliations: Universitat Pompeu Fabra (ES)
ORCID: Mann, Christopher J
Perdiguero, Eusebio
Kharraz, Yacine
Pessina, Patrizia
Serrano, Antonio L
Venue: Skeletal Muscle
Publisher: Springer Science and Business Media LLC
Published: 2011-05-04
Volume: 1
Issue: 1
Pages: 21-21
ISSN: 2044-5040 (ISSN-L)
DOI: 10.1186/2044-5040-1-21
PMC: PMC3156644
OpenAlex: W2076787014
Cited by: 853
References: 129
Citations by year: 2026: 37 · 2025: 59 · 2024: 55 · 2023: 53 · 2022: 59 · 2021: 71 · 2020: 81 · 2019: 85 · 2018: 76 · 2017: 51 · 2016: 68 · 2015: 48 · 2014: 49 · 2013: 33 · 2012: 27
FWCI: 14.30
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Skeletal Muscle (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
RECERCAT (Consorci de Serveis Universitaris de Catalunya) (publishedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion, cc-by)
Funders: Ministerio de Ciencia e Innovación (PLE2009)
Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
Health Sciences › Medicine › Surgery › Wound Healing and Treatments
Keywords: muscle fibrosis, muscle repair, muscular dystrophy, satellite cells, muscle stem cells, fibroblast activation, inflammatory cell infiltration, extracellular matrix, wound healing, microenvironment

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Aberrant repair and fibrosis development in skeletal muscle

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