Distinct Phases of Postnatal Skeletal Muscle Growth Govern the Progressive Establishment of Muscle Stem Cell Quiescence

Gattazzo, Francesca; Laurent, Béatrice; Relaix, Frédéric; Rouard, Hélène; Didier, Nathalie

doi:10.1016/j.stemcr.2020.07.011

Cited by 66 publications

(57 citation statements)

References 39 publications

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“…It is also known that miR-1 and −206 suppress Pax7 expression and act as regulators of satellite cell proliferation and differentiation (80). Postnatal muscle hypertrophy may also be regulated by satellite cell number per fibre at birth and their rate of proliferation as well as protein deposition (i.e., protein synthesis and degradation) (82). Therefore, our future studies will focus on satellite cells which will be assessed in histological sections.…”

Section: Discussionmentioning

confidence: 99%

Small-RNA sequencing reveals altered skeletal muscle microRNAs and snoRNAs signatures in weanling male offspring from mouse dams fed a low protein diet during lactation

Kanakis

Alameddine

Folkes

et al. 2021

Preprint

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Nutrition plays a key role in pre- and postnatal growth of the musculoskeletal system. Maternal diet during gestation and lactation affects the development of skeletal muscles in the offspring and determines muscle health in later life, however, the molecular mechanisms that govern these effects are largely unknown. In this study, we aim to describe the association between maternal low protein diet-induced changes in offspring skeletal muscle and the differential expression (DE) of small non-coding RNAs (sncRNAs). We used a mouse model of maternal protein restriction to characterise the impact of early-life undernutrition on skeletal muscle morphology in male offspring at weaning. Mouse dams were fed either a normal (N, 20%) or a low protein (L, 8%) diet during gestation and newborn pups were cross-fostered to N or L lactating dams, resulting in the generation of NN, NL and LN offspring groups. Total body and tibialis anterior (TA) weights were decreased in NL males but not different in the LN group, as compared to NN, although neonates from low protein fed dams were smaller at birth than those born to dams fed a normal protein. However, histological evaluation of TA muscle revealed reduced muscle fibre size in both groups at the end of lactation. Small RNA-seq analysis demonstrated DE of multiple classes of sncRNAs, including miRs, snoRNAs and snRNAs. Bioinformatic analyses of miRs-15a, -34a, -122 and -199a, in combination with known myomiRs, confirmed their implication in key muscle-specific biological processes and cellular functions and suggest a promising set of miRs in muscle physiology studies. To our knowledge, this is the first comprehensive report for the DE of sncRNAs in nutrition-associated programming of skeletal muscle development, highlighting the need for further research.

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Section: Discussionmentioning

confidence: 99%

Small-RNA sequencing reveals altered skeletal muscle microRNAs and snoRNAs signatures in weanling male offspring from mouse dams fed a low protein diet during lactation

Kanakis

Alameddine

Folkes

et al. 2021

Preprint

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“…Myonuclear accretion during juvenile muscle development continues up to at least 6 weeks of age (puberty onset) in the mouse, and early adolescence in humans 30,44,[53][54][55] . The adult quiescent SC pool is not fully established until young adult age, and contribution of active SCs is necessary for prepubertal myofiber growth 30,56 . Prepubertal SC ablation leaves both the adult EDL and SOL muscles with reduced myofiber size and myonuclear number 30 .…”

Section: Discussionmentioning

confidence: 99%

Chemoradiation impairs myofiber hypertrophic growth in a pediatric tumor model

Paris

Kallenbach

Bachman

et al. 2020

Sci Rep

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Pediatric cancer treatment often involves chemotherapy and radiation, where off-target effects can include skeletal muscle decline. The effect of such treatments on juvenile skeletal muscle growth has yet to be investigated. We employed a small animal irradiator to administer fractionated hindlimb irradiation to juvenile mice bearing implanted rhabdomyosarcoma (RMS) tumors. Hindlimb-targeted irradiation (3 × 8.2 Gy) of 4-week-old mice successfully eliminated RMS tumors implanted one week prior. After establishment of this preclinical model, a cohort of tumor-bearing mice were injected with the chemotherapeutic drug, vincristine, alone or in combination with fractionated irradiation (5 × 4.8 Gy). Single myofiber analysis of fast-contracting extensor digitorum longus (EDL) and slow-contracting soleus (SOL) muscles was conducted 3 weeks post-treatment. Although a reduction in myofiber size was apparent, EDL and SOL myonuclear number were differentially affected by juvenile irradiation and/or vincristine treatment. In contrast, a decrease in myonuclear domain (myofiber volume/myonucleus) was observed regardless of muscle or treatment. Thus, inhibition of myofiber hypertrophic growth is a consistent feature of pediatric cancer treatment.

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“…Cells were washed with HBSS, and then fixed and permeabilized in 500 µL of Fixation solution (Transcription buffer set, BD Biosciences) for 45 min at +4 °C, in accordance with manufacturer’s instructions. Fixed cells were washed with the Permeabilization/Wash buffer (Transcription buffer set, BD Pharmingen) and proceeded for nuclear immunostaining as previously reported [ 23 ]. The following mix of conjugated antibodies was used: mouse anti-PAX3/7-AF647 (B-5) (Santa Cruz, Dallas, TX, USA #sc-365843), mouse anti-MYOD-PE (BD Biosciences, #554130, custom made coupling by manufacturer), mouse anti-MYOG-AF488 (5FD) (Santa Cruz, #sc-52903), mouse anti-KI67-bV421 (BD Biosciences, #562899).…”

Section: Methodsmentioning

confidence: 99%

“…The following mix of conjugated antibodies was used: mouse anti-PAX3/7-AF647 (B-5) (Santa Cruz, Dallas, TX, USA #sc-365843), mouse anti-MYOD-PE (BD Biosciences, #554130, custom made coupling by manufacturer), mouse anti-MYOG-AF488 (5FD) (Santa Cruz, #sc-52903), mouse anti-KI67-bV421 (BD Biosciences, #562899). Specificity of the staining was verified using isotypic controls for each antibody [ 23 ]. Cells were washed with the Permeabilization/Wash solution, re-suspended in HBSS and transferred in BD Trucount TM Absolute Counting Tubes (BD Biosciences, #340334) before being analyzed using a BD FACS Canto TM Flow Cytometer (BD Biosciences).…”

Section: Methodsmentioning

confidence: 99%

Progressive and Coordinated Mobilization of the Skeletal Muscle Niche throughout Tissue Repair Revealed by Single-Cell Proteomic Analysis

Borok

Didier

Gattazzo

et al. 2021

Cells

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Background: Skeletal muscle is one of the only mammalian tissues capable of rapid and efficient regeneration after trauma or in pathological conditions. Skeletal muscle regeneration is driven by the muscle satellite cells, the stem cell population in interaction with their niche. Upon injury, muscle fibers undergo necrosis and muscle stem cells activate, proliferate and fuse to form new myofibers. In addition to myogenic cell populations, interaction with other cell types such as inflammatory cells, mesenchymal (fibroadipogenic progenitors—FAPs, pericytes) and vascular (endothelial) lineages are important for efficient muscle repair. While the role of the distinct populations involved in skeletal muscle regeneration is well characterized, the quantitative changes in the muscle stem cell and niche during the regeneration process remain poorly characterized. Methods: We have used mass cytometry to follow the main muscle cell types (muscle stem cells, vascular, mesenchymal and immune cell lineages) during early activation and over the course of muscle regeneration at D0, D2, D5 and D7 compared with uninjured muscles. Results: Early activation induces a number of rapid changes in the proteome of multiple cell types. Following the induction of damage, we observe a drastic loss of myogenic, vascular and mesenchymal cell lineages while immune cells invade the damaged tissue to clear debris and promote muscle repair. Immune cells constitute up to 80% of the mononuclear cells 5 days post-injury. We show that muscle stem cells are quickly activated in order to form new myofibers and reconstitute the quiescent muscle stem cell pool. In addition, our study provides a quantitative analysis of the various myogenic populations during muscle repair. Conclusions: We have developed a mass cytometry panel to investigate the dynamic nature of muscle regeneration at a single-cell level. Using our panel, we have identified early changes in the proteome of stressed satellite and niche cells. We have also quantified changes in the major cell types of skeletal muscle during regeneration and analyzed myogenic transcription factor expression in satellite cells throughout this process. Our results highlight the progressive dynamic shifts in cell populations and the distinct states of muscle stem cells adopted during skeletal muscle regeneration. Our findings give a deeper understanding of the cellular and molecular aspects of muscle regeneration.

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Distinct Phases of Postnatal Skeletal Muscle Growth Govern the Progressive Establishment of Muscle Stem Cell Quiescence

Cited by 66 publications

References 39 publications

Small-RNA sequencing reveals altered skeletal muscle microRNAs and snoRNAs signatures in weanling male offspring from mouse dams fed a low protein diet during lactation

Small-RNA sequencing reveals altered skeletal muscle microRNAs and snoRNAs signatures in weanling male offspring from mouse dams fed a low protein diet during lactation

Chemoradiation impairs myofiber hypertrophic growth in a pediatric tumor model

Progressive and Coordinated Mobilization of the Skeletal Muscle Niche throughout Tissue Repair Revealed by Single-Cell Proteomic Analysis

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