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The roles of miRNAs in adult skeletal muscle satellite cells

FREE RADICAL BIOLOGY AND MEDICINE (2023)

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Senescence atlas reveals an aged-like inflamed niche that blunts muscle regeneration

Victoria Moiseeva et al.

Summary: This study reveals that senescent cells are crucial components of the skeletal muscle regenerative niche and inhibit regeneration. Through single-cell transcriptomics and senescent-cell enrichment sorting, different types of senescent cells were identified and isolated from damaged muscles of young and old mice. The findings demonstrate that senescent cells create an aged-like inflamed niche and impair stem cell proliferation and regeneration.

NATURE (2023)

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Article Multidisciplinary Sciences

Decrease in the expression of muscle-specific miRNAs, miR-133a and miR-1, in myoblasts with replicative senescence

Kaori Shintani-Ishida et al.

Summary: Injured or aging muscles undergo myogenic regeneration, but aging impairs the function of myoblasts, which play a crucial role in this process. MicroRNAs (miRNAs), specifically miR-1 and miR-133a, also contribute to myogenic regeneration by controlling the proliferation and differentiation of myoblasts. However, the expression of miR-1 and miR-133a is altered in senescent myoblasts, leading to impaired myogenic differentiation. Treatment with a glutaminase 1 inhibitor can improve this dysfunction by removing senescent cells and increasing miR-133a expression. Similar alterations in miRNA expression were observed in myoblasts from aged mice compared to younger mice. These findings suggest that replicative senescence suppresses muscle-specific miRNA expression, contributing to the dysfunction in myogenic regeneration.

PLOS ONE (2023)

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Article Cell Biology

MicroRNA control of the myogenic cell transcriptome and proteome: the role of miR-16

Seongkyun Lim et al.

Summary: MicroRNA-16 (miR-16) plays a crucial role in stem cell biology and fate. It is lowly expressed in muscle during developmental hypertrophy and regeneration, and its inhibition enhances myoblast differentiation and myotube formation. Global transcriptomic and proteomic analyses revealed that miR-16 knockdown affects ribosomal protein gene expression, p53 pathway-related gene abundance, and regulation of tricarboxylic acid (TCA) cycle proteins and RNA metabolism-related proteins. miR-16 inhibition also induces specific proteins associated with myogenic differentiation. Overall, miR-16 is involved in myogenic cell differentiation.

AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY (2023)

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Review Cell Biology

The life and times of cellular senescence in skeletal muscle: friend or foe for homeostasis and adaptation?

Cory M. Dungan et al.

Summary: A decline in skeletal muscle mass and function is linked to increased mortality and disease risk during aging. Exercise training is most effective in enhancing muscle health, but older individuals have reduced adaptive response and muscle repair potential. Accumulation of senescent cells in muscle is implicated as a contributing factor to aging phenotype. It is important to study the prevalence and consequences of senescent cells in muscle for understanding muscle aging and potential interventions.

AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY (2023)

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Article Cell Biology

Multiomics reveals glutathione metabolism as a driver of bimodality during stem cell aging

Daniel I. Benjamin et al.

Summary: With age, skeletal muscle stem cells (MuSCs) exhibit slower activation and increased death, resulting in defective muscle repair. Through multiomics, single-cell measurements, and functional testing, researchers have identified perturbed glutathione (GSH) metabolism as a mechanism of MuSC aging. This perturbed metabolism leads to a dichotomy in the aged MuSC population, with some cells maintaining functionality and others having impaired functionality due to reduced GSH levels. Manipulating GSH levels can alter the functional dichotomy and potentially reverse MuSC aging.

CELL METABOLISM (2023)

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Skeletal muscle-enriched miRNAs are highly unstable in vivo and may be regulated in a Dicer-independent manner

Satoshi Oikawa et al.

Summary: MicroRNAs (miRNAs) are stably expressed in skeletal muscle, but their half-lives are relatively short, ranging from 11 to 20 hours. The stability of skeletal-muscle-enriched miRNAs in vivo is lower than expected. Furthermore, a Dicer-independent biogenetic pathway may contribute to the production of mature miRNAs.

FEBS JOURNAL (2023)

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Review Biochemistry & Molecular Biology

Regenerating Myofibers after an Acute Muscle Injury: What Do We Really Know about Them?

Francis X. Pizza et al.

Summary: Injury to skeletal muscle initiates muscle regeneration, which involves the formation of regenerating myofibers with central myonuclei. However, little is known about the maturation process of regenerating myofibers into normal-sized myofibers with peripheral myonuclei. This review compares and contrasts myofiber maturation during muscle development and regeneration, aiming to identify unique cellular and molecular processes of myofiber maturation in muscle regeneration.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2023)

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Article Multidisciplinary Sciences

miR-378 influences muscle satellite cells and enhances adipogenic potential of fibro-adipogenic progenitors but does not affect muscle regeneration in the glycerol-induced injury model

Olga Mucha et al.

Summary: Skeletal muscle regeneration is influenced by the interaction between different types of cells. Deletion of miR-378 affects the abundance of muscle satellite cells and the adipogenic potential of fibro-adipogenic progenitors, but does not impact overall regeneration upon acute glycerol-induced muscle injury.

SCIENTIFIC REPORTS (2023)

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Review Endocrinology & Metabolism

The pentose phosphate pathway in health and disease

Tara Teslaa et al.

Summary: The pentose phosphate pathway (PPP) is a glucose-oxidizing pathway that produces ribose 5-phosphate and NADPH. It plays a critical role in suppressing oxidative stress and supports the generation of reactive species for signaling and pathogen killing. Genetic deficiencies in the PPP, particularly in glucose-6-phosphate dehydrogenase (G6PD), can lead to hemolytic anemia and infections. This review comprehensively discusses the role of PPP in biochemistry, physiology, and disease.

NATURE METABOLISM (2023)

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Article Biochemistry & Molecular Biology

Propolis Ethanolic Extract Attenuates D-gal-induced C2C12 Cell Injury by Modulating Nrf2/HO-1 and p38/p53 Signaling Pathways

Songhao Tian et al.

Summary: This study investigated the effect of propolis ethanolic extract (PEE) on D-galactose-induced damage in mouse C2C12 cells. The results showed that PEE increased cell viability, decreased senescence-associated beta-galactosidase-positive cells, and promoted cell differentiation. PEE protected cells from oxidative stress by activating the Nrf2/HO-1 signaling pathway, and inhibited apoptosis by suppressing p38 phosphorylation and reducing p53 expression. These findings provide a theoretical basis for the use of PEE in alleviating muscle atrophy.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2023)

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Control of satellite cell function in muscle regeneration and its disruption in ageing

Pedro Sousa-Victor et al.

Summary: Satellite cells are skeletal muscle stem cells that are mostly dormant and reactivate upon muscle damage. Their activation and differentiation are regulated by intrinsic and niche signals, with age-related deregulation leading to impaired muscle regeneration.

NATURE REVIEWS MOLECULAR CELL BIOLOGY (2022)

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Review Biochemistry & Molecular Biology

Insights into muscle stem cell dynamics during postnatal development

John F. Bachman et al.

Summary: During development, resident stem cell populations contribute to the growth and maturation of tissue and organs. In skeletal muscle, muscle stem cells play a key role in the maturation of postnatal myofibers. The timing of when these stem cells enter a mature quiescent state and the implications of their loss or dysfunction during development stages are still under debate.

FEBS JOURNAL (2022)

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Article Biochemistry & Molecular Biology

Cellular Senescence and Aging in Myotonic Dystrophy

Yuhei Hasuike et al.

Summary: Myotonic dystrophy is a genetic disorder affecting multiple organs with clinical similarities to aging. Cellular senescence plays a key role in the pathogenesis of myotonic dystrophy.

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miR-486 is essential for muscle function and suppresses a dystrophic transcriptome

Adrienne Samani et al.

Summary: miR-486 plays a significant role in muscle function, with reduced expression associated with Duchenne muscular dystrophy. It is essential for normal muscle function and contributes to pathological remodeling in dystrophin-deficient muscle. Additionally, it serves as a useful biomarker for disease progression. The use of multiple omic platforms is effective in identifying in vivo miR-486 target transcripts.

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A glitch in the matrix: the pivotal role for extracellular matrix remodeling during muscle hypertrophy

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Extracellular vesicle-derived miRNAs improve stem cell-based therapeutic approaches in muscle wasting conditions

Laura Yedigaryan et al.

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MicroRNA cargo of extracellular vesicles released by skeletal muscle fibro-adipogenic progenitor cells is significantly altered with disuse atrophy and IL-1b deficiency

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Control of CRK-RAC1 activity by the miR-1/206/133 miRNA family is essential for neuromuscular junction function

Ina Klockner et al.

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The mitochondrial protein OPA1 regulates the quiescent state of adult muscle stem cells

Nicole Baker et al.

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Multi-transcriptome analysis following an acute skeletal muscle growth stimulus yields tools for discerning global and MYC regulatory networks

Kevin A. Murach et al.

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Article Cell Biology

NRF2 Regulates Viability, Proliferation, Resistance to Oxidative Stress, and Differentiation of Murine Myoblasts and Muscle Satellite Cells

Iwona Bronisz-Budzynska et al.

Summary: Increased oxidative stress can hinder skeletal muscle regeneration and affect muscle satellite cells (mSCs) activity. NRF2 transcription factor plays an important role in muscle cell biology by promoting myoblast proliferation and viability, reducing reactive oxygen species production, and inhibiting myoblast differentiation. NRF2 is also crucial for the viability of mSCs.

CELLS (2022)

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Characterization of cellular senescence in aging skeletal muscle

Xu Zhang et al.

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NATURE AGING (2022)

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Review Endocrinology & Metabolism

Extracellular Vesicles as Communicators of Senescence in Musculoskeletal Aging

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microRNAstrand selection: Unwinding the rules

Jeffrey C. Medley et al.

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WILEY INTERDISCIPLINARY REVIEWS-RNA (2021)

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miR-24 and its target gene Prdx6 regulate viability and senescence of myogenic progenitors during aging

Ana Soriano-Arroquia et al.

Summary: The decline in satellite cell-dependent skeletal muscle regeneration with aging is associated with alterations in miR-24 expression and its target gene Prdx6. Changes in miR-24 levels impact mitochondrial ROS generation, DNA damage pathways, and the viability and myogenic potential of myogenic progenitors, with more pronounced effects observed in old mice. The downregulation of miR-24 and subsequent upregulation of Prdx6 in response to aging may represent an adaptive mechanism to maintain satellite cell function in muscle.

AGING CELL (2021)

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Dicer-mediated miRNA processing is not involved in controlling muscle mass during muscle atrophy

Satoshi Oikawa et al.

Summary: The study showed that knockout of Dicer in adult skeletal muscle did not affect denervation-induced muscle atrophy.

SCIENTIFIC REPORTS (2021)

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Targeting microRNA-mediated gene repression limits adipogenic conversion of skeletal muscle mesenchymal stromal cells

Michael N. Wosczyna et al.

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CELL STEM CELL (2021)

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The Effects of Muscle Cell Aging on Myogenesis

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INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Evidence of myomiR regulation of the pentose phosphate pathway during mechanical load-induced hypertrophy

Taylor Valentino et al.

Summary: The research identifies the molecular and cellular mechanisms regulating skeletal muscle hypertrophy using the rodent synergist ablation model, and examines the metabolic pathways in muscle during mechanical overload (MOV) through gene expression analysis. The study suggests that enhanced redox metabolism via NADPH production may play a key role in muscle hypertrophy induced by MOV, potentially regulated by a myomiR network.

PHYSIOLOGICAL REPORTS (2021)

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MiR-34a suppression targets Nampt to ameliorate bone marrow mesenchymal stem cell senescence by regulating NAD+-Sirt1 pathway

Chenchen Pi et al.

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STEM CELL RESEARCH & THERAPY (2021)

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Early satellite cell communication creates a permissive environment for long-term muscle growth

Kevin A. Murach et al.

Summary: The study demonstrates that satellite cells communicate with other cells in skeletal muscle during mechanical overload, affecting proper long-term extracellular matrix deposition. They modulate chemokine gene expression and influence cell phenotype through extracellular vesicle delivery of miR-206.

ISCIENCE (2021)

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Human muscle stem cells are refractory to aging

James S. Novak et al.

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AGING CELL (2021)

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Extracellular vesicles released from stress-induced prematurely senescent myoblasts impair endothelial function and proliferation

Zachary R. Hettinger et al.

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EXPERIMENTAL PHYSIOLOGY (2021)

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Fusion and beyond: Satellite cell contributions to loading-induced skeletal muscle adaptation

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ARCHIVES OF BIOCHEMISTRY AND BIOPHYSICS (2017)

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miR-16 controls myoblast proliferation and apoptosis through directly suppressing Bcl2 and FOXO1 activities

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BIOCHIMICA ET BIOPHYSICA ACTA-GENE REGULATORY MECHANISMS (2017)

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Myogenic Progenitor Cells Control Extracellular Matrix Production by Fibroblasts during Skeletal Muscle Hypertrophy

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Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts

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AUTOPHAGY (2016)

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BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS (2016)

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NEUROCHEMICAL RESEARCH (2016)

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Conditional Loss of Pten in Myogenic Progenitors Leads to Postnatal Skeletal Muscle Hypertrophy but Age-Dependent Exhaustion of Satellite Cells

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NUCLEIC ACIDS RESEARCH (2012)

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microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7

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MicroRNA-206 Delays ALS Progression and Promotes Regeneration of Neuromuscular Synapses in Mice

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2007)

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MIR-206 regulates connexin43 expression during skeletal muscle development

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Muscle-specific microRNA miR-206 promotes muscle differentiation

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The satellite cell as a companion in skeletal muscle plasticity: currency, conveyance, clue, connector and colander

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Myogenic factors that regulate expression of muscle-specific, microRNAs

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NATURE GENETICS (2006)

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Article Multidisciplinary Sciences

Somitic origin of limb muscle satellite and side population cells

J Schienda et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2006)

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Article Multidisciplinary Sciences

Structural basis for double-stranded RNA processing by dicer

IJ MacRae et al.

SCIENCE (2006)

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Article Cell Biology

Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis

S Kuang et al.

JOURNAL OF CELL BIOLOGY (2006)

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Article Cell Biology

Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells

F Relaix et al.

JOURNAL OF CELL BIOLOGY (2006)

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Article Multidisciplinary Sciences

Silencing of microRNAs in vivo with 'antagomirs'

J Krützfeldt et al.

NATURE (2005)

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Article Multidisciplinary Sciences

A Pax3/Pax7-dependent population of skeletal muscle progenitor cells

F Relaix et al.

NATURE (2005)

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Article Cell Biology

Pax3/Pax7 mark a novel population of primitive myogenic cells during development

L Kassar-Duchossoy et al.

GENES & DEVELOPMENT (2005)

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Article Cell Biology

Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing

C Kanellopoulou et al.

GENES & DEVELOPMENT (2005)

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Letter Biochemistry & Molecular Biology

Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets

BP Lewis et al.

CELL (2005)

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Article Biochemistry & Molecular Biology

Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs

MT Bohnsack et al.

RNA (2004)

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Article Biochemistry & Molecular Biology

Identification of mammalian microRNA host genes and transcription units

A Rodriguez et al.

GENOME RESEARCH (2004)

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Article Biotechnology & Applied Microbiology

Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation

LF Sempere et al.

GENOME BIOLOGY (2004)

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Article Cell Biology

Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs

R Yi et al.

GENES & DEVELOPMENT (2003)

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Article Genetics & Heredity

Dicer is essential for mouse development

E Bernstein et al.

NATURE GENETICS (2003)

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Article Biochemistry & Molecular Biology

Reversal of human cellular senescence:: roles of the p53 and p16 pathways

CM Beauséjour et al.

EMBO JOURNAL (2003)

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Article Biochemistry & Molecular Biology

New microRNAs from mouse and human

M Lagos-Quintana et al.

RNA (2003)

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Article Biochemistry & Molecular Biology

Identification of tissue-specific microRNAs from mouse

M Lagos-Quintana et al.

CURRENT BIOLOGY (2002)

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Article Biochemistry & Molecular Biology

Peptide elongation factor eEF1A-2/S1 expression in cultured differentiated myotubes and its protective effect against caspase-3-mediated apoptosis

LB Ruest et al.

JOURNAL OF BIOLOGICAL CHEMISTRY (2002)

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Article Multidisciplinary Sciences

Identification of novel genes coding for small expressed RNAs

M Lagos-Quintana et al.

SCIENCE (2001)

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Article Multidisciplinary Sciences

An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans

NC Lau et al.

SCIENCE (2001)

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Article Multidisciplinary Sciences

An extensive class of small RNAs in Caenorhabditis elegans

RC Lee et al.

SCIENCE (2001)

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Article Multidisciplinary Sciences

Role for a bidentate ribonuclease in the initiation step of RNA interference

E Bernstein et al.

NATURE (2001)

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Article Multidisciplinary Sciences

Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA

AE Pasquinelli et al.

NATURE (2000)

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Article Biochemistry & Molecular Biology

Pax7 is required for the specification of myogenic satellite cells

P Seale et al.

CELL (2000)

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