Clonal analysis reveals a common origin between nonsomite-derived neck muscles and heart myocardium

Lescroart, Fabienne; Hamou, Wissam; Francou, Alexandre; Théveniau-Ruissy, Magali; Kelly, Robert G.; Buckingham, Margaret

doi:10.1073/pnas.1424538112

Cited by 108 publications

(149 citation statements)

References 44 publications

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“…Facial-expression muscles, derived from the second branchial arches, are clonally related to the outflow region of the heart, to myocardium at the base of the pulmonary trunk and the aorta. A third sublineage forms the nonsomitic muscles of the neck, notably the trapezius and sternocleidomastoid muscles, and including muscles of the larynx and the nonsomitic component of the splenius muscle (16). This finding is in keeping with observations of Pax3 independence and Tbx1 dependence of the trapezius and sternocleidomastoid muscles (34).…”

Section: Cell Lineage Analysessupporting

confidence: 83%

“…In the case of second arch derivatives, this segregation correlates with left-hand clones that also colonize the base of the pulmonary trunk, whereas clones on the righthand side of the face colonize the base of the aorta (10). Similarly for trapezius and sternocleidomastoid neck muscles, left/ right labeling correlates with clones in the left part of the venous pole-the left atrium, left superior caval vein, and pulmonary vein, as well as the pulmonary trunk at the venous pole-vs. right-hand labeling in the right atrium and right superior caval vein (16). This left/right segregation takes place at the onset of gastrulation (36).…”

Section: Cell Lineage Analysesmentioning

confidence: 95%

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Gene regulatory networks and cell lineages that underlie the formation of skeletal muscle

Buckingham

2017

Proc. Natl. Acad. Sci. U.S.A.

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Skeletal muscle in vertebrates is formed by two major routes, as illustrated by the mouse embryo. Somites give rise to myogenic progenitors that form all of the muscles of the trunk and limbs. The behavior of these cells and their entry into the myogenic program is controlled by gene regulatory networks, where paired box gene 3 (Pax3) plays a predominant role. Head and some neck muscles do not derive from somites, but mainly form from mesoderm in the pharyngeal region. Entry into the myogenic program also depends on the myogenic determination factor (MyoD) family of genes, but Pax3 is not expressed in these myogenic progenitors, where different gene regulatory networks function, with T-box factor 1 (Tbx1) and paired-like homeodomain factor 2 (Pitx2) as key upstream genes. The regulatory genes that underlie the formation of these muscles are also important players in cardiogenesis, expressed in the second heart field, which is a major source of myocardium and of the pharyngeal arch mesoderm that gives rise to skeletal muscles. The demonstration that both types of striated muscle derive from common progenitors comes from clonal analyses that have established a lineage tree for parts of the myocardium and different head and neck muscles. Evolutionary conservation of the two routes to skeletal muscle in vertebrates extends to chordates, to trunk muscles in the cephlochordate Amphioxus and to muscles derived from cardiopharyngeal mesoderm in the urochordate Ciona, where a related gene regulatory network determines cardiac or skeletal muscle cell fates. In conclusion, Eric Davidson's visionary contribution to our understanding of gene regulatory networks and their evolution is acknowledged.skeletal myogenesis | muscle origins | second heart field | gene regulatory networks | cell lineages M ovement is a fundamental requirement for animal survival, both for finding food/feeding and for avoiding predators/ locating to a propitious environment, and depends on cells with contractile properties, mainly based on actomyosin motor activity. In more sophisticated organisms, specialized contractile proteins are present in muscle cells. In vertebrates, striated muscle permits movement and also underlies the pumping activity of the heart, which, like the simpler peristaltic pumps present in the vascular system of many animals, performs a vital function in ensuring the circulation of nutrients within the body. Striated muscles contain a range of distinct and overlapping contractile protein isoforms, adapted to functional requirements of the motor activity of different skeletal muscles or of contractility in different cardiac compartments of the heart. Although the contractile apparatus is similar at the protein level, the upstream regulation of cardiac or skeletal muscle genes is different. Skeletal muscle formation depends on myogenic regulatory factors of the myogenic determination factor (MyoD) family, whereas in cardiac muscle, these basic helix-loop-helix factors do not play a role, and other families of transcription factors...

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Section: Cell Lineage Analysessupporting

confidence: 83%

Section: Cell Lineage Analysesmentioning

confidence: 95%

Gene regulatory networks and cell lineages that underlie the formation of skeletal muscle

Buckingham

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…the right ventricle and outflow tract) share a common origin with branchiomeric head muscles, in the cardiopharyngeal mesoderm of the early embryo (Diogo et al, 2015a;Gopalakrishnan et al, 2015;Harel et al, 2012;Lescroart et al, 2010Lescroart et al, , 2014Lescroart et al, , 2015Mandal et al, 2017;Nathan et al, 2008;Tirosh-Finkel et al, 2006;Tzahor and Evans, 2011) .…”

Section: Introductionmentioning

confidence: 99%

A single cell transcriptional roadmap for cardiopharyngeal fate diversification

Wang

Niu

Jullian

et al. 2017

Preprint

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SummaryDynamic gene expression programs determine multipotent cell states and fate choices during development. Multipotent progenitors for cardiomyocytes and branchiomeric head muscles populate the pharyngeal mesoderm of vertebrate embryos, but the mechanisms underlying cardiopharyngeal multipotency and heart vs. head muscle fate choices remain elusive. The tunicate Ciona emerged as a simple chordate model to study cardiopharyngeal development with unprecedented spatio-temporal resolution. We analyzed the transcriptome of single cardiopharyngeal lineage cells isolated at successive time points encompassing the transitions from multipotent progenitors to distinct first and second heart, and pharyngeal muscle precursors. We reconstructed the three cardiopharyngeal developmental trajectories, and characterized gene expression dynamics and regulatory states underlying each fate choice.Experimental perturbations and bulk transcriptome analyses revealed that ongoing FGF/MAPK signaling maintains cardiopharyngeal multipotency and promotes the pharyngeal muscle fate, whereas signal termination permits the deployment of a full pan-cardiac program and heart fate specification. We identified the Dach1/2 homolog as a novel evolutionarily conserved second-heart-field-specific factor and demonstrate, through lineage tracing and CRISPR/Cas9 perturbations, that it operates downstream of Tbx1/10 to actively suppress the first heart lineage program. This data indicates that the regulatory state of multipotent cardiopharyngeal progenitors determines the first vs. second heart lineage choice, and that Tbx1/10 acts as a bona fide regulator of cardiopharyngeal multipotency.2 All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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“…Neck muscles, located in the transition zone between head and trunk, have both somitic and nonsomitic origins. The trapezius and sternocleidomastoid neck muscle (also termed the cucullaris muscle in jawed vertebrates) progenitor cells express markers of the pharyngeal mesoderm (PM), indicating their branchiomeric origin, whereas other muscles in the neck are derived from Pax3 + somitic cells (Lescroart et al, 2015;Theis et al, 2010). Likewise, homotopic and heterotopic transplantation experiments in the chick revealed that the occipital lateral plate mesoderm (LPM) (adjacent to somites 1-3) gives rise to neck muscles (Theis et al, 2010).…”

Section: S3mentioning

confidence: 99%

“…Likewise, homotopic and heterotopic transplantation experiments in the chick revealed that the occipital lateral plate mesoderm (LPM) (adjacent to somites 1-3) gives rise to neck muscles (Theis et al, 2010). Recent retrospective clonal analysis in the mouse embryo shows that a distinct subpopulation within the PM contributes to the formation of the trapezius muscle as well as to the myocardium at the venous pole of the heart (IFT, inflow tract) (Lescroart et al, 2015). This study demonstrates that while there is a clonal relationship between the trapezius and sternocleidomastoid muscles and the laryngeal muscles (both muscles that derived from the posterior pharyngeal arches (PAs) 3-6), there is no clonal relation with other head or somite-derived muscles.…”

Section: S3mentioning

confidence: 99%