Developmental origins of species-specific muscle pattern

Tokita, Masayuki; Schneider, Richard A.

doi:10.1016/j.ydbio.2009.05.548

Cited by 69 publications

(90 citation statements)

References 129 publications

(155 reference statements)

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“…In vertebrates, skeletal muscles which form in the head, trunk and limbs are patterned by extrinsic cues from surrounding tissues to adopt specific arrangements of muscle fibres in the adult form [23][24][25][26][27][28][29][30][31] . For example, somite-derived limb muscle precursor cells migrate into the limb bud which is filled with lateral platederived connective tissue.…”

Section: Discussionmentioning

confidence: 99%

The developmental basis of bat wing muscle

2012

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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.

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Section: Discussionmentioning

confidence: 99%

The developmental basis of bat wing muscle

2012

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“…Neural crest (NC) cells that migrate out of the caudal midbrain and rostral hindbrain are the only source of skeletogenic mesenchyme within the mandibular primordia (Couly et al, 1993;Köntges and Lumsden, 1996;Le Lièvre and Douarin, 1975;Noden, 1978;Noden and Schneider, 2006). Previous work has shown that the orchestration of developmental programs regulating jaw size is under the regulatory control of NC Jheon and Schneider, 2009;Schneider, 2005;Schneider and Helms, 2003;Tokita and Schneider, 2009), but how NC achieves this complex task remains unclear.…”

Section: Research Articlementioning

confidence: 99%

Multiple developmental mechanisms regulate species-specific jaw size

et al. 2014

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Variation in jaw size during evolution has been crucial for the adaptive radiation of vertebrates, yet variation in jaw size during development is often associated with disease. To test the hypothesis that early developmental events regulating neural crest (NC) progenitors contribute to species-specific differences in size, we investigated mechanisms through which two avian species, duck and quail, achieve their remarkably different jaw size. At early stages, duck exhibit an anterior shift in brain regionalization yielding a shorter, broader, midbrain. We find no significant difference in the total number of pre-migratory NC; however, duck concentrate their premigratory NC in the midbrain, which contributes to an increase in size of the post-migratory NC population allocated to the mandibular arch. Subsequent differences in proliferation lead to a progressive increase in size of the duck mandibular arch relative to that of quail. To test the role of pre-migratory NC progenitor number in regulating jaw size, we reduced and augmented NC progenitors. In contrast to previous reports of regeneration by NC precursors, we find that neural fold extirpation results in a loss of NC precursors. Despite this reduction in their numbers, post-migratory NC progenitors compensate, producing a symmetric and normal-sized jaw. Our results suggest that evolutionary modification of multiple aspects of NC cell biology, including NC allocation within the jaw primordia and NC-mediated proliferation, have been important to the evolution of jaw size. Furthermore, our finding of NC post-migratory compensatory mechanisms potentially extends the developmental time frame for treatments of disease or injury associated with NC progenitor loss.

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“…We previously demonstrated that head muscle patterning and differentiation are governed by the interaction of head muscle progenitors with the adjacent CNC cells (Rinon et al, 2007;Tzahor et al, 2003). Therefore, CNC cells impose anatomical features of the musculoskeletal architecture upon their neighbors (Grenier et al, 2009;Heude et al, 2010;Rinon et al, 2007;Tokita and Schneider, 2009).…”

Section: Introductionmentioning

confidence: 99%

p53 coordinates cranial neural crest cell growth and epithelial-mesenchymal transition/delamination processes

et al. 2011

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SUMMARYNeural crest development involves epithelial-mesenchymal transition (EMT), during which epithelial cells are converted into individual migratory cells. Notably, the same signaling pathways regulate EMT function during both development and tumor metastasis. p53 plays multiple roles in the prevention of tumor development; however, its precise roles during embryogenesis are less clear. We have investigated the role of p53 in early cranial neural crest (CNC) development in chick and mouse embryos. In the mouse, p53 knockout embryos displayed broad craniofacial defects in skeletal, neuronal and muscle tissues. In the chick, p53 is expressed in CNC progenitors and its expression decreases with their delamination from the neural tube. Stabilization of p53 protein using a pharmacological inhibitor of its negative regulator, MDM2, resulted in reduced SNAIL2 (SLUG) and ETS1 expression, fewer migrating CNC cells and in craniofacial defects. By contrast, electroporation of a dominant-negative p53 construct increased PAX7 + SOX9 + CNC progenitors and EMT/delamination of CNC from the neural tube, although the migration of these cells to the periphery was impaired. Investigating the underlying molecular mechanisms revealed that p53 coordinates CNC cell growth and EMT/delamination processes by affecting cell cycle gene expression and proliferation at discrete developmental stages; disruption of these processes can lead to craniofacial defects.

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Developmental origins of species-specific muscle pattern

Cited by 69 publications

References 129 publications

The developmental basis of bat wing muscle

The developmental basis of bat wing muscle

Multiple developmental mechanisms regulate species-specific jaw size

p53 coordinates cranial neural crest cell growth and epithelial-mesenchymal transition/delamination processes

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