How to make a tongue: Cellular and molecular regulation of muscle and connective tissue formation during mammalian tongue development

Cobourne, Martyn T.; Iseki, Sachiko; Birjandi, Anahid A.; Al-Lami, Hadeel Adel; Thauvin‐Robinet, Christel; Xavier, Guilherme M.; Liu, Karen

doi:10.1016/j.semcdb.2018.04.016

Cited by 25 publications

(32 citation statements)

References 65 publications

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“…Tongue anomalies are a common finding amongst the multiple defects that can affect the developing craniofacial region (Cobourne et al, 2019). In this study, we have investigated the temporospatial contribution of SHH signalling in the developing tongue through the analysis of multiple mouse mutants.…”

Section: Discussionmentioning

confidence: 99%

Temporospatial sonic hedgehog signalling is essential for neural crest-dependent patterning of the intrinsic tongue musculature

et al. 2019

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The tongue is a highly specialised muscular organ with a complex anatomy required for normal function. We have utilised multiple genetic approaches to investigate local temporospatial requirements for sonic hedgehog (SHH) signalling during tongue development. Mice lacking a Shh cis-enhancer, MFCS4 (ShhMFCS4/−), with reduced SHH in dorsal tongue epithelium have perturbed lingual septum tendon formation and disrupted intrinsic muscle patterning, with these defects reproduced following global Shh deletion from E10.5 in pCag-CreERTM; Shhflox/flox embryos. SHH responsiveness was diminished in local cranial neural crest cell (CNCC) populations in both mutants, with SHH targeting these cells through the primary cilium. CNCC-specific deletion of orofaciodigital syndrome 1 (Ofd1), which encodes a ciliary protein, in Wnt1-Cre; Ofdfl/Y mice led to a complete loss of normal myotube arrangement and hypoglossia. In contrast, mesoderm-specific deletion of Ofd1 in Mesp1-Cre; Ofdfl/Y embryos resulted in normal intrinsic muscle arrangement. Collectively, these findings suggest key temporospatial requirements for local SHH signalling in tongue development (specifically, lingual tendon differentiation and intrinsic muscle patterning through signalling to CNCCs) and provide further mechanistic insight into the tongue anomalies seen in patients with disrupted hedgehog signalling.

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Section: Discussionmentioning

confidence: 99%

Temporospatial sonic hedgehog signalling is essential for neural crest-dependent patterning of the intrinsic tongue musculature

et al. 2019

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“…Furthermore, the expression of Dx5/6 in neural crest-derived cells closely associated with the masseter suggested that Dlx5/6 + MCT in particular may be critical for masseter morphogenesis. Finally, multiple studies have shown that signals from the neural crest are critical for several aspects of tongue muscle development (reviewed by Cobourne et al, 2018). The first step in tongue development is the migration of muscle progenitors following the migration of neural crest cells to the tongue bud (Han et al, 2012).…”

Section: Cranial Musclementioning

confidence: 99%

Connecting muscle development, birth defects, and evolution: An essential role for muscle connective tissue

Sefton

Kardon

2019

Current Topics in Developmental Biology

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Skeletal muscle powers all movement of the vertebrate body and is distributed in multiple regions that have evolved distinct functions. Axial muscles are ancestral muscles essential for support and locomotion of the whole body. The evolution of the head was accompanied by development of cranial muscles essential for eye movement, feeding, vocalization, and facial expression. With the evolution of paired fins and limbs and their associated muscles, vertebrates gained increased locomotor agility, populated the land, and acquired fine motor skills. Finally, unique muscles with specialized functions have evolved in some groups, and the diaphragm which solely evolved in mammals to increase respiratory capacity is one such example. The function of all these muscles requires their integration with the other components of the musculoskeletal system: muscle connective tissue (MCT), tendons, bones as well as nerves and vasculature. MCT is muscle’s closest anatomical and functional partner. Not only is MCT critical in the adult for muscle structure and function, but recently MCT in the embryo has been found to be crucial for muscle development. In this review, we examine the important role of the MCT in axial, head, limb, and diaphragm muscles for regulating normal muscle development, discuss how defects in MCT-muscle interactions during development underlie the etiology of a range of birth defects, and explore how changes in MCT development or communication with muscle may have led to the modification and acquisition of new muscles during vertebrate evolution.

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“…Subsequently, the hypopharyngeal eminence overgrows the copula, which in turn disappears progressively. Consequently, the rostral part of the hypopharyngeal eminence develops into the posterior third of the tongue [ 2 , 3 , 4 ]. Thus, the embryonic origin in the anterior two-thirds and posterior third of the tongue differs.…”

Section: Introductionmentioning

confidence: 99%

SoxGenes Show Spatiotemporal Expression during Murine Tongue and Eyelid Development

Ishikawa

Kawasaki

et al. 2018

International Journal of Dentistry

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The tongue is a critical organ, involved in functions such as speaking, swallowing, mastication, and degustation. Although Sox genes are known to play critical roles in many biological processes, including organogenesis, the expression of the Sox family members during tongue development remains unclear. We therefore performed a comparative in situ hybridization analysis of 17 Sox genes (Sox1–14, 17, 18, and 21) during murine tongue development. Sox2, 4, 6, 8, 9, 10, 11, 12, and 21 were found to be expressed in the tongue epithelium, whereas Sox2, 4–6, 8–11, 13, and 21 showed expression in the mesenchyme of the developing tongue. Expression of Sox1, 4, 6, 8–12, and 21 were observed in the developing tongue muscle. Sox5 and 13 showed expression only at E12, while Sox1 expression was observed only on E18. Sox6, 8, 9, and 12 showed expression at several stages. Although the expression of Sox2, 4, 10, 11, and 21 was detected during all the four stages of tongue development, their expression patterns differed among the stages. We thus identified a dynamic spatiotemporal expression pattern of the Sox genes during murine tongue development. To understand whether Sox genes are involved in the development of other craniofacial organs through similar roles to those in tongue development, we also examined the expression of Sox genes in eyelid primordia, which also contain epithelium, mesenchyme, and muscle. However, expression patterns and timing of Sox genes differed between tongue and eyelid development. Sox genes are thus related to organogenesis through different functions in each craniofacial organ.

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How to make a tongue: Cellular and molecular regulation of muscle and connective tissue formation during mammalian tongue development

Cited by 25 publications

References 65 publications

Temporospatial sonic hedgehog signalling is essential for neural crest-dependent patterning of the intrinsic tongue musculature

Temporospatial sonic hedgehog signalling is essential for neural crest-dependent patterning of the intrinsic tongue musculature

Connecting muscle development, birth defects, and evolution: An essential role for muscle connective tissue

SoxGenes Show Spatiotemporal Expression during Murine Tongue and Eyelid Development

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