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Extraocular muscle satellite cells are high performance myo-engines retaining efficient regenerative capacity in dystrophin deficiency.

作者信息

Stuelsatz Pascal, Shearer Andrew, Li Yunfei, Muir Lindsey A, Ieronimakis Nicholas, Shen Qingwu W, Kirillova Irina, Yablonka-Reuveni Zipora

机构信息

Department of Biological Structure, University of Washington School of Medicine, Seattle, WA, USA.

Program in Molecular and Cellular Biology and Department of Neurology, University of Washington School of Medicine, Seattle, WA, USA.

出版信息

Dev Biol. 2015 Jan 1;397(1):31-44. doi: 10.1016/j.ydbio.2014.08.035. Epub 2014 Sep 16.


DOI:10.1016/j.ydbio.2014.08.035
PMID:25236433
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC4309674/
Abstract

Extraocular muscles (EOMs) are highly specialized skeletal muscles that originate from the head mesoderm and control eye movements. EOMs are uniquely spared in Duchenne muscular dystrophy and animal models of dystrophin deficiency. Specific traits of myogenic progenitors may be determinants of this preferential sparing, but very little is known about the myogenic cells in this muscle group. While satellite cells (SCs) have long been recognized as the main source of myogenic cells in adult muscle, most of the knowledge about these cells comes from the prototypic limb muscles. In this study, we show that EOMs, regardless of their distinctive Pax3-negative lineage origin, harbor SCs that share a common signature (Pax7(+), Ki67(-), Nestin-GFP(+), Myf5(nLacZ+), MyoD-positive lineage origin) with their limb and diaphragm somite-derived counterparts, but are remarkably endowed with a high proliferative potential as revealed in cell culture assays. Specifically, we demonstrate that in adult as well as in aging mice, EOM SCs possess a superior expansion capacity, contributing significantly more proliferating, differentiating and renewal progeny than their limb and diaphragm counterparts. These robust growth and renewal properties are maintained by EOM SCs isolated from dystrophin-null (mdx) mice, while SCs from muscles affected by dystrophin deficiency (i.e., limb and diaphragm) expand poorly in vitro. EOM SCs also retain higher performance in cell transplantation assays in which donor cells were engrafted into host mdx limb muscle. Collectively, our study provides a comprehensive picture of EOM myogenic progenitors, showing that while these cells share common hallmarks with the prototypic SCs in somite-derived muscles, they distinctively feature robust growth and renewal capacities that warrant the title of high performance myo-engines and promote consideration of their properties for developing new approaches in cell-based therapy to combat skeletal muscle wasting.

摘要

相似文献

[1]
Extraocular muscle satellite cells are high performance myo-engines retaining efficient regenerative capacity in dystrophin deficiency.

Dev Biol. 2015-1-1

[2]
Fetal skeletal muscle progenitors have regenerative capacity after intramuscular engraftment in dystrophin deficient mice.

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[3]
Ancestral Myf5 gene activity in periocular connective tissue identifies a subset of fibro/adipogenic progenitors but does not connote a myogenic origin.

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[4]
Isolation of Mouse Periocular Tissue for Histological and Immunostaining Analyses of the Extraocular Muscles and Their Satellite Cells.

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[5]
A new immuno-, dystrophin-deficient model, the NSG-mdx(4Cv) mouse, provides evidence for functional improvement following allogeneic satellite cell transplantation.

Stem Cells. 2013-8

[6]
Isolation, Culture, and Immunostaining of Skeletal Muscle Myofibers from Wildtype and Nestin-GFP Mice as a Means to Analyze Satellite Cell.

Methods Mol Biol. 2017

[7]
Heme Oxygenase-1 Influences Satellite Cells and Progression of Duchenne Muscular Dystrophy in Mice.

Antioxid Redox Signal. 2018-5-23

[8]
Dystrophic changes in extraocular muscles after gamma irradiation in mdx:utrophin(+/-) mice.

PLoS One. 2014-1-21

[9]
Interplay between Pitx2 and Pax7 temporally governs specification of extraocular muscle stem cells.

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[10]
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引用本文的文献

[1]
Regulatory Landscapes of Muscle Satellite Cells: From Mechanism to Application.

Int J Stem Cells. 2025-8-30

[2]
Interplay between Pitx2 and Pax7 temporally governs specification of extraocular muscle stem cells.

PLoS Genet. 2024-6

[3]
Extreme Tolerance of Extraocular Muscles to Diseases and Aging: Why and How?

Int J Mol Sci. 2024-5-3

[4]
Distinct transcriptomic profile of satellite cells contributes to preservation of neuromuscular junctions in extraocular muscles of ALS mice.

Elife. 2024-4-25

[5]
Cellular pathogenesis of Duchenne muscular dystrophy: progressive myofibre degeneration, chronic inflammation, reactive myofibrosis and satellite cell dysfunction.

Eur J Transl Myol. 2023-10-16

[6]
Stem cells and extracellular vesicles to improve preclinical orofacial soft tissue healing.

Stem Cell Res Ther. 2023-8-15

[7]
Extracellular Matrix Proteomics: The Mouse Diaphragm as a Surrogate for Studying Myofibrosis in Dystrophinopathy.

Biomolecules. 2023-7-12

[8]
Fibrotic remodeling and tissue regeneration mechanisms define the therapeutic potential of human muscular progenitors.

Bioeng Transl Med. 2022-11-26

[9]
Biomedical applications of three-dimensional bioprinted craniofacial tissue engineering.

Bioeng Transl Med. 2022-5-10

[10]
Fibroadipogenic Progenitors Regulate the Basal Proliferation of Satellite Cells and Homeostasis of Pharyngeal Muscles via HGF Secretion.

Front Cell Dev Biol. 2022-5-17

本文引用的文献

[1]
Muscle structure influences utrophin expression in mdx mice.

PLoS Genet. 2014-6-12

[2]
Notch signaling deficiency underlies age-dependent depletion of satellite cells in muscular dystrophy.

Dis Model Mech. 2014-8

[3]
Dystrophic changes in extraocular muscles after gamma irradiation in mdx:utrophin(+/-) mice.

PLoS One. 2014-1-21

[4]
Satellite cells: the architects of skeletal muscle.

Curr Top Dev Biol. 2014

[5]
Ancestral Myf5 gene activity in periocular connective tissue identifies a subset of fibro/adipogenic progenitors but does not connote a myogenic origin.

Dev Biol. 2013-8-19

[6]
Lying low but ready for action: the quiescent muscle satellite cell.

FEBS J. 2013-7-12

[7]
A new immuno-, dystrophin-deficient model, the NSG-mdx(4Cv) mouse, provides evidence for functional improvement following allogeneic satellite cell transplantation.

Stem Cells. 2013-8

[8]
Gene and cell-mediated therapies for muscular dystrophy.

Muscle Nerve. 2013-3-29

[9]
The role of Pitx2 in maintaining the phenotype of myogenic precursor cells in the extraocular muscles.

PLoS One. 2013-3-7

[10]
Moderate-intensity treadmill running promotes expansion of the satellite cell pool in young and old mice.

FEBS J. 2013-4-12

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