Muscle contraction is required to maintain the pool of muscle progenitors via YAP and NOTCH during fetal myogenesis

Lima, Joana Esteves de; Bonnin, Marie-Ange; Birchmeier, Carmen; Duprez, Delphine

doi:10.7554/elife.15593

Cited by 72 publications

(85 citation statements)

References 78 publications

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“…In mouse studies, muscle progenitor cells expressing ERBB3 or NGFR are responsive to paracrine signals secreted by neural crest or neuronal cells 46,47 . During hPSC directed differentiation, SMPCs may be supported by a local micro-environment that includes three dimensional cellular structures and neuronal cells 48 .As several biological processes associated with neuronal cells and transmission of neural impulses were identified by RNA-SEQ in hPSC-SMPC cultures, we expect that neuronal cells are important for hPSC myogenesis throughout directed differentiation.…”

Section: Discussionmentioning

confidence: 99%

ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs

et al. 2017

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Human pluripotent stem cells (hPSCs) can be directed to differentiate into skeletal muscle progenitor cells (SMPCs). However, the myogenicity of hPSC-SMPCs relative to human fetal or adult satellite cells remains unclear. HPSC-SMPCs derived by directed differentiation are less functional in vitro and in vivo compared to human satellite cells. Utilizing RNA-SEQ, we identified cell surface receptors ERBB3 and NGFR that demarcate myogenic populations, including PAX7 progenitors in human fetal development and hPSC-SMPCs. We demonstrated that hPSC skeletal muscle is immature, but inhibition of TGF-β signaling during differentiation improved fusion efficiency, ultrastructural organization, and expression of adult myosins. This enrichment and maturation strategy restored dystrophin in hundreds of dystrophin-deficient myofibers after engraftment of CRISPR/Cas9-corrected Duchenne muscular dystrophy hiPSC-SMPCs. The work provides an in-depth characterization of human myogenesis, and identifies candidates that improve the in vivo myogenic potential of hPSC-SMPCs to levels equal to directly-isolated human fetal muscle cells.

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Section: Discussionmentioning

confidence: 99%

ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs

et al. 2017

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“…Instead, it could act in a mechanism influencing the differentiation of these cell types. Although not explored here, previous studies suggest a role for Yap in ciliogenesis and in the regulation of Notch, a known determinant of cell fate decisions in the airway epithelium (de Lima et al, 2016;Grampa et al, 2016;Kim et al, 2015;Mahoney et al, 2014;Totaro et al, 2017;Tschaharganeh et al, 2013;Tu et al, 2018;Yimlamai et al, 2014).…”

Section: Dynamic Patterns Of Yap Subcellular Localization During Distmentioning

confidence: 93%

Yap and its subcellular localization have distinct compartment-specific roles in the developing lung

Soldt

Qian

et al. 2019

Development

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Although the Hippo-yes-associated protein (Yap) pathway has been implicated in lung development, the specific roles for Yap and its nucleocytoplasmic shuttling in the developing airway and alveolar compartments remain elusive. Moreover, conflicting results from expression studies and differences in the lung phenotypes of Yap and Hippo kinase null mutants caused controversy over the dynamics and significance of Yap subcellular localization in the developing lung.Here, we show that the aberrant morphogenesis of Yap-deficient lungs results from the disruption of developmental events specifically in distal epithelial progenitors. We also show that activation of nuclear Yap is enough to fulfill the Yap requirements to rescue abnormalities in these lungs. Remarkably, we found that Yap nucleocytoplasmic shuttling is largely dispensable in epithelial progenitors for both branching morphogenesis and sacculation. However, if maintained transcriptionally active in airways, nuclear Yap profoundly alters proximal-distal identity and halts epithelial differentiation. Taken together, these observations provide novel insights into the crucial importance of Hippo-Yap signaling in the lung prenatally.

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“…We also confirmed that MyHC-emb is not expressed by myogenic progenitors or myoblasts and is only expressed by myofibers, implying that the observed effect on differentiation has to be non-cell autonomous, where signals from the myofibers lacking MyHCemb lead to rapid rate of differentiation of the myogenic progenitors, depleting the myogenic progenitor pool. Interestingly, a recent study reported that the Pax7+ muscle stem cell pool and its differentiation is regulated by signals from the differentiated myofibers, including mechanical forces of muscle contraction (Esteves de Lima, et al, 2016).…”

Section: Myhc-embryonic Is a Key Regulator Of Embryonic And Fetal Mymentioning

confidence: 99%

Myosin Heavy Chain-embryonic is a crucial regulator of skeletal muscle development and differentiation

Sharma

Agarwal

Kumar³

et al. 2018

Preprint

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SummaryMyosin heavy chains (MyHCs) are contractile proteins that are part of the thick filaments of the functional unit of the skeletal muscle, the sarcomere. In addition to MyHCs that are part of the adult muscle contractile network, two MyHCs -MyHC-embryonic and -perinatal are expressed during muscle development and are only transiently expressed in the adult during regeneration.The functions performed by these MyHCs has been a long-standing question and using a targeted mouse allele, we have characterized the role of MyHC-embryonic. Analysis of loss-of-function mice reveals that lack of MyHC-embryonic leads to mis-regulation of other MyHCs, alterations in fiber size, fiber number and fiber type at neonatal stages. We also find that loss of MyHCembryonic leads to mis-regulation of genes involved in muscle differentiation. A broad theme from these studies is that loss of MyHC-embryonic has distinct effects on different muscles, possibly reflecting the unique fiber type composition of different muscles. Most significantly, our results indicate that MyHC-embryonic is required during embryonic and fetal myogenesis to regulate myogenic progenitor and myoblast differentiation in a non-cell autonomous manner via Mitogen Activated Protein Kinase (MAPKinase) and Fibroblast Growth Factor (FGF) signaling. Thus, our results signify that MyHC-embryonic is a key regulator of myogenic differentiation during embryonic, fetal and neonatal myogenesis.

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Muscle contraction is required to maintain the pool of muscle progenitors via YAP and NOTCH during fetal myogenesis

Cited by 72 publications

References 78 publications

ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs

ERBB3 and NGFR mark a distinct skeletal muscle progenitor cell in human development and hPSCs

Yap and its subcellular localization have distinct compartment-specific roles in the developing lung

Myosin Heavy Chain-embryonic is a crucial regulator of skeletal muscle development and differentiation

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