A Cranial Mesoderm Origin for Esophagus Striated Muscles

Gopalakrishnan, Swetha; Comai, Glenda; Sambasivan, Ramkumar; Francou, Alexandre; Kelly, Robert G.; Tajbakhsh, Shahragim

doi:10.1016/j.devcel.2015.07.003

Cited by 61 publications

(81 citation statements)

References 51 publications

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“…In mice, Tbx1 regulates Myf5 and MyoD in the myogenic branchial arch mesoderm (Sambasivan et al, 2009), and is required for formation of striated esophageal muscles, both of which derive from Mesp1+ cardiopharyngeal mesoderm (Gopalakrishnan et al, 2015). Indeed, it has been proposed that the Mesp+ B7.5 lineage is homologous to the vertebrate cardiopharyngeal mesoderm (Stolfi et al, 2010;Wang et al, 2013;Kaplan et al, 2015;Diogo et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Rewiring of an ancestral Tbx1/10-Ebf-Mrf network for pharyngeal muscle specification in distinct embryonic lineages

Tolkin

Christiaen

2016

Development

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Skeletal muscles arise from diverse embryonic origins in vertebrates, yet converge on extensively shared regulatory programs that require muscle regulatory factor (MRF)-family genes. Myogenesis in the tail of the simple chordate Ciona exhibits a similar reliance on its single MRF-family gene, and diverse mechanisms activate Ci-Mrf. Here, we show that myogenesis in the atrial siphon muscles (ASMs) and oral siphon muscles (OSMs), which control the exhalant and inhalant siphons, respectively, also requires Mrf. We characterize the ontogeny of OSM progenitors and compare the molecular basis of Mrf activation in OSM versus ASM. In both muscle types, Ebf and Tbx1/10 are expressed and function upstream of Mrf. However, we demonstrate that regulatory relationships between Tbx1/10, Ebf and Mrf differ between the OSM and ASM lineages. We propose that Tbx1, Ebf and Mrf homologs form an ancient conserved regulatory state for pharyngeal muscle specification, whereas their regulatory relationships might be more evolutionarily variable.

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Section: Discussionmentioning

confidence: 99%

Rewiring of an ancestral Tbx1/10-Ebf-Mrf network for pharyngeal muscle specification in distinct embryonic lineages

Tolkin

Christiaen

2016

Development

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“…This movement is in contrast to the migration of isolated progenitor cells from trunk somites to the diaphragm or limbs. Nonsomitic muscles differentiate during fetal stages, so that most head muscles are clearly distinguishable at embryonic day 14.5 (E14.5) in the mouse embryo (10), and the esophagus skeletal muscle is only laid down at E15.5 (8). This process differs from the first skeletal muscles of the trunk, the myotomes, which form immediately adjacent to the somites from E8.5 (1).…”

Section: Skeletal Muscles Of the Head And Neckmentioning

confidence: 99%

“…The skeletal muscle of the mammalian esophagus is also of nonsomitic origin. Myogenic progenitors from the pharyngeal region colonize this structure, moving posteriorly along the smooth muscle layer into the body from the early fetal stage (8). Somitic cells that have moved anteriorly after delamination contribute to some muscles positioned in the head region, as seen for intrinsic laryngeal and tongue muscles that derive from myogenic cells in the hypoglossal chord, a structure formed from the hypaxial region of occipital somites.…”

Section: Skeletal Muscles Of the Head And Neckmentioning

confidence: 99%

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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“…The additional postnatal cranioskeletal anomalies that we have described may reflect a combination of primary and secondary effects. It is unlikely that BA-derived muscles have a cellautonomous requirement for Hmx1, as we have shown that dmECR activity and Hmx1 protein expression do not overlap the staining of Isl1, a marker for mesodermally derived muscle precursors in BA1 and BA2 (Nathan et al, 2008;Gopalakrishnan et al, 2015), which give rise to many muscles of the head and neck (Rinon et al, 2007). However, in dumbo animals, muscle attachment sites, such as the paired bony paraoccipital processes, are significantly hypoplastic.…”

Section: Discussionmentioning

confidence: 89%

“…In order to determine whether Hmx1 directly contributes to either muscle or nerve development and organization, we performed immunohistochemistry for Isl1, a known marker for muscle precursors in BA2 (Nathan et al, 2008;Gopalakrishnan et al, 2015), and for neurofilament. Using dmECR-driven lacZ activity as a proxy for endogenous Hmx1 (see below), we found that Hmx1 was not present in muscle precursor cells (Fig.…”

Section: Hmx1mentioning

confidence: 99%

A distal 594bp ECR specifies Hmx1 expression in pinna and lateral facial morphogenesis and is regulated by Hox-Pbx-Meis

Rosin

Cox

et al. 2016

Development

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Hmx1 encodes a homeodomain transcription factor expressed in the developing lateral craniofacial mesenchyme, retina and sensory ganglia. Mutation or mis-regulation of Hmx1 underlies malformations of the eye and external ear in multiple species. Deletion or insertional duplication of an evolutionarily conserved region (ECR) downstream of Hmx1 has recently been described in rat and cow, respectively. Here, we demonstrate that the impact of Hmx1 loss is greater than previously appreciated, with a variety of lateral cranioskeletal defects, auriculofacial nerve deficits, and duplication of the caudal region of the external ear. Using a transgenic approach, we demonstrate that a 594 bp sequence encompassing the ECR recapitulates specific aspects of the endogenous Hmx1 lateral facial expression pattern. Moreover, we show that Hoxa2, Meis and Pbx proteins act cooperatively on the ECR, via a core 32 bp sequence, to regulate Hmx1 expression. These studies highlight the conserved role for Hmx1 in BA2-derived tissues and provide an entry point for improved understanding of the causes of the frequent lateral facial birth defects in humans.

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A Cranial Mesoderm Origin for Esophagus Striated Muscles

Cited by 61 publications

References 51 publications

Rewiring of an ancestral Tbx1/10-Ebf-Mrf network for pharyngeal muscle specification in distinct embryonic lineages

Rewiring of an ancestral Tbx1/10-Ebf-Mrf network for pharyngeal muscle specification in distinct embryonic lineages

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

A distal 594bp ECR specifies Hmx1 expression in pinna and lateral facial morphogenesis and is regulated by Hox-Pbx-Meis

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