Collier/OLF/EBF-Dependent Transcriptional Dynamics Control Pharyngeal Muscle Specification from Primed Cardiopharyngeal Progenitors

Razy-Krajka, Florian; Lam, Karen; Wang, Wei; Stolfi, Alberto; Joly, Marine; Bonneau, Richard; Christiaen, Lionel

doi:10.1016/j.devcel.2014.04.001

Cited by 101 publications

(242 citation statements)

References 75 publications

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“…As is the case in other invertebrates, the Ciona genome encodes a single MRF-family bHLH transcription factor. However, as is the case in vertebrates, Mrf is expressed in all committed muscle precursors: the primary and secondary tail muscles, atrial siphon muscles (ASMs) and oral siphon muscles (OSMs) (Meedel et al, 2007;Razy-Krajka et al, 2014). Another similarity with vertebrates is that Mrf expression and muscle differentiation in Ciona seem to be regulated differently depending on the embryonic origin of the muscle cells.…”

Section: Introductionmentioning

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: Introductionmentioning

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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“…NK4/Nkx2.5 was recently shown to antagonize Tbx1 and repress EBF/COE function to promote cardiac versus pharyngeal muscle fate in the ascidian SHF, with Islet1 being expressed in both derivatives (Wang et al, 2013;Razy-Krajka et al, 2014). In the Drosophila embryo, the orthologs of Nkx2.5 and Islet1 are required for the formation of all (in the case of Tin) or some (in the case of Tup) of the dorsal mesodermal derivatives (heart, dorsal body wall muscles, visceral muscles, lymph gland) (Azpiazu and Frasch, 1993;Bodmer, 1993;Zaffran et al, 2006;Mann et al, 2009).…”

Section: Direct Regulation Of Tup By Org-1 Is Am/tarm-specificmentioning

confidence: 99%

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

et al. 2014

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The T-box transcription factor Tbx1 and the LIM-homeodomain transcription factor Islet1 are key components in regulatory circuits that generate myogenic and cardiogenic lineage diversity in chordates. We show here that Org-1 and Tup, the Drosophila orthologs of Tbx1 and Islet1, are co-expressed and required for formation of the heart-associated alary muscles (AMs) in the abdomen. The same holds true for lineage-related muscles in the thorax that have not been described previously, which we name thoracic alary-related muscles (TARMs). Lineage analyses identified the progenitor cell for each AM and TARM. Three-dimensional highresolution analyses indicate that AMs and TARMs connect the exoskeleton to the aorta/heart and to different regions of the midgut, respectively, and surround-specific tracheal branches, pointing to an architectural role in the internal anatomy of the larva. Org-1 controls tup expression in the AM/TARM lineage by direct binding to two regulatory sites within an AM/TARM-specific cis-regulatory module, tupAME. The contributions of Org-1 and Tup to the specification of Drosophila AMs and TARMs provide new insights into the transcriptional control of Drosophila larval muscle diversification and highlight new parallels with gene regulatory networks involved in the specification of cardiopharyngeal mesodermal derivatives in chordates.

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“…We photoconverted a nuclear version of Kaede (Razy-Krajka et al, 2014) in the founder cells to test whether their initial arrangement prefigures leader versus trailer selection (Fig. 1M,N).…”

Section: −21mentioning

confidence: 99%

“…Statistical analyses were performed in Excel and GraphPadPrism. Kaede was converted using the 405 nm diode laser of the inverted TCS SP8 X confocal microscope as described previously (Razy-Krajka et al, 2014).…”

Section: Confocal Imaging Kaede Photoconversion and Image Analysismentioning

confidence: 99%

Surrounding tissues canalize motile cardiopharyngeal progenitors towards collective polarity and directed migration

et al. 2015

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Collectively migrating cells maintain group polarity and interpret external cues to reach their destination. The cardiogenic progenitors (also known as trunk ventral cells, TVCs) of the ascidian Ciona intestinalis provide a simple chordate model with which to study collective migration. Bilateral pairs of associated TVCs undergo a stereotyped polarized migration away from the tail towards the ventral trunk, arguably constituting the simplest possible example of directed collective migration. To identify tissues contributing to TVC polarity and migration, we quantified the contact between TVCs and surrounding tissues, and blocked the secretory pathway in a tissuespecific manner. Even though TVCs normally migrate as an invariably determined leader-trailer polarized pair of adherent cells, they are capable of migrating individually, albeit a shorter distance and with altered morphology. The mesenchyme contacts newborn TVCs and contributes to robust specification of the trailer but appears to have only minor effects on directed migration. The notochord does not contact the TVCs but contributes to the onset of migration. The trunk endoderm first contacts the leader TVC, then 'encases' both migrating cells and provides the inputs maintaining leader-trailer polarity. Migrating TVCs adhere to the epidermis and need this contact for their cohesion. These phenomenological studies reveal that inherently motile cardiopharyngeal progenitors are channeled into stereotyped behaviors by interactions with surrounding tissues.

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Collier/OLF/EBF-Dependent Transcriptional Dynamics Control Pharyngeal Muscle Specification from Primed Cardiopharyngeal Progenitors

Cited by 101 publications

References 75 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

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

Surrounding tissues canalize motile cardiopharyngeal progenitors towards collective polarity and directed migration

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