Sonic hedgehog acts cell-autonomously on muscle precursor cells to generate limb muscle diversity

Anderson, Charles L.; Williams, Victoria C.; Moyon, Benjamin; Daubas, Philippe; Tajbakhsh, Shahragim; Buckingham, Margaret; Shiroishi, Toshihiko; Hughes, Simon M.; Borycki, Anne‐Gaëlle

doi:10.1101/gad.187807.112

Cited by 50 publications

(43 citation statements)

References 82 publications

(83 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Although molecular mechanisms controlling the organization of skeletal muscle in space during vertebrate development are not fully understood, signalling molecules secreted from non-myogenic mesenchyme or muscle connective tissue, as well as cell adhesion molecules localized at the cell membrane of muscle connective tissue, potentially affect the architectural pattern of muscles 21,22,30,[40][41][42][43][44][45][46][47][48] . In tongue morphogenesis, cranial neural crest-derived tongue muscle connective tissue is required for organizing occipital somite-derived tongue muscle cells 49 .…”

Section: Discussionmentioning

confidence: 99%

The developmental basis of bat wing muscle

2012

View full text Add to dashboard Cite

By acquiring wings, bats are the only mammalian lineage to have achieved flight. To be capable of powered flight, they have unique muscles associated with their wing. However, the developmental origins of bat wing muscles, and the underlying molecular and cellular mechanisms are unknown. Here we report, first, that the wing muscles are derived from multiple myogenic sources with different embryonic origins, and second, that there is a spatiotemporal correlation between the outgrowth of wing membranes and the expansion of wing muscles into them. Together, these findings imply that the wing membrane itself may regulate the patterning of wing muscles. Last, through comparative gene expression analysis, we show Fgf10 signalling is uniquely activated in the primordia of wing membranes. Our results demonstrate how components of Fgf signalling are likely to be involved in the development and evolution of novel complex adaptive traits.

show abstract

Section: Discussionmentioning

confidence: 99%

The developmental basis of bat wing muscle

2012

View full text Add to dashboard Cite

show abstract

“…Immunodetection was performed as previously described (Hinits et al, 2009;Anderson et al, 2012). Alkaline phosphatase was revealed after antibody staining by washing into PBS and 2 mM MgCl 2 at 65°C for 30 minutes, transferring into 100 mM NaCl, 100 mM Tris-Cl (pH 9.5), 50 mM MgCl 2 , 0.1% Tween and 2 mM levamisole for 20 minutes, and developing in NBT/BCIP (Roche).…”

Section: In Situ Hybridisation and Immunohistochemistrymentioning

confidence: 99%

Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion

et al. 2013

Self Cite

View full text Add to dashboard Cite

Striated muscles that enable mouth opening and swallowing during feeding are essential for efficient energy acquisition, and are likely to have played a fundamental role in the success of early jawed vertebrates. The developmental origins and genetic requirements of these muscles are uncertain. Here, we determine by indelible lineage tracing in mouse that fibres of sternohyoid muscle (SHM), which is essential for mouth opening during feeding, and oesophageal striated muscle (OSM), which is crucial for voluntary swallowing, arise from Pax3-expressing somite cells. In vivo Kaede lineage tracing in zebrafish reveals the migratory route of cells from the anteriormost somites to OSM and SHM destinations. Expression of pax3b, a zebrafish duplicate of Pax3, is restricted to the hypaxial region of anterior somites that generate migratory muscle precursors (MMPs), suggesting that Pax3b plays a role in generating OSM and SHM. Indeed, loss of pax3b function led to defective MMP migration and OSM formation, disorganised SHM differentiation, and inefficient ingestion and swallowing of microspheres. Together, our data demonstrate Pax3-expressing somite cells as a source of OSM and SHM fibres, and highlight a conserved role of Pax3 genes in the genesis of these feeding muscles of vertebrates.

show abstract

“…In zebrafish, different levels and durations of Shh signaling specify distinct myotomal cell types (Feng et al, 2006;Hammond et al, 2007;Ingham and McMahon, 2001;Maurya et al, 2011;Wolff et al, 2003). In the chick, Shh was found to be necessary for epaxial but not limb muscle formation (Teillet et al, 1998), yet studies in mouse propose that it induces the myogenic program in the ventral limb (Anderson et al, 2012;Hu et al, 2012;Krüger et al, 2001). In addition, Shh has been shown to regulate Myf5 expression in primary epaxial RESEARCH ARTICLE Sonic hedgehog in myotome development myoblasts (Borycki et al, 1999;Chiang et al, 1996;Gustafsson et al, 2002), although other studies do not support this finding (Teboul et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

The transition from differentiation to growth during dermomyotome-derived myogenesis depends on temporally restricted hedgehog signaling

et al. 2013

View full text Add to dashboard Cite

SUMMARYThe development of a functional tissue requires coordination of the amplification of progenitors and their differentiation into specific cell types. The molecular basis for this coordination during myotome ontogeny is not well understood. Dermomytome progenitors that colonize the myotome first acquire myocyte identity and subsequently proliferate as Pax7-expressing progenitors before undergoing terminal differentiation. We show that the dynamics of sonic hedgehog (Shh) signaling is crucial for this transition in both avian and mouse embryos. Initially, Shh ligand emanating from notochord/floor plate reaches the dermomyotome, where it both maintains the proliferation of dermomyotome cells and promotes myogenic differentiation of progenitors that colonized the myotome. Interfering with Shh signaling at this stage produces small myotomes and accumulation of Pax7-expressing progenitors. An in vivo reporter of Shh activity combined with mouse genetics revealed the existence of both activator and repressor Shh activities operating on distinct subsets of cells during the epaxial myotomal maturation. In contrast to observations in mice, in avians Shh promotes the differentiation of both epaxial and hypaxial myotome domains. Subsequently, myogenic progenitors become refractory to Shh; this is likely to occur at the level of, or upstream of, smoothened signaling. The end of responsiveness to Shh coincides with, and is thus likely to enable, the transition into the growth phase of the myotome.

show abstract

Sonic hedgehog acts cell-autonomously on muscle precursor cells to generate limb muscle diversity

Cited by 50 publications

References 82 publications

The developmental basis of bat wing muscle

The developmental basis of bat wing muscle

Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion

The transition from differentiation to growth during dermomyotome-derived myogenesis depends on temporally restricted hedgehog signaling

Contact Info

Product

Resources

About