Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity

Ruest, L. Bruno; Xiang, Xilin; Lim, Kim Chew; Levi, Giovanni; Clouthier, David E.

doi:10.1242/dev.01291

Cited by 138 publications

(242 citation statements)

References 71 publications

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“…Further transformations about the hinge are seen with the targeted disruption of both the endothelin signaling pathway and its potential targets, the nested Dlx5 and Dlx6 genes (Kurihara et al, 1994;Clouthier et al, 1998;Yanagisawa et al, 1998;Acampora et al, 1999;Depew et al, 1999;Charite et al, 2001;Ruest et al, 2004). Dlx5 is expressed both in early head mesenchyme (mdBA1 CNC) and epithelia (e.g., the early anterior cephalic ectoderm, ANR, and olfactory and otic placodes; Simeone et al, 1994;Qiu et al, 1997;Yang et al, 1998;Depew et al, 1999).…”

Section: Figmentioning

confidence: 99%

21^st Century neontology and the comparative development of the vertebrate skull

Depew

Simpson

2006

Developmental Dynamics

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Classic neontology (comparative embryology and anatomy), through the application of the concept of homology, has demonstrated that the development of the gnathostome (jawed vertebrate) skull is characterized both by a fidelity to the gnathostome bauplan and the exquisite elaboration of final structural design. Just as homology is an old concept amended for modern purposes, so are many of the questions regarding the development of the skull. With due deference to Geoffroy-St. Hilaire, Cuvier, Owen, Lankester et al., we are still asking: How are bauplan fidelity and elaboration of design maintained, coordinated, and modified to generate the amazing diversity seen in cranial morphologies? What establishes and maintains pattern in the skull? Are there universal developmental mechanisms underlying gnathostome autapomorphic structural traits? Can we detect and identify the etiologies of heterotopic (change in the topology of a developmental event), heterochronic (change in the timing of a developmental event), and heterofacient (change in the active capacetence, or the elaboration of capacity, of a developmental event) changes in craniofacial development within and between taxa? To address whether jaws are all made in a like manner (and if not, then how not), one needs a starting point for the sake of comparison. To this end, we present here a "hinge and caps" model that places the articulation, and subsequently the polarity and modularity, of the upper and lower jaws in the context of cranial neural crest competence to respond to positionally located epithelial signals. This model expands on an evolving model of polarity within the mandibular arch and seeks to explain a developmental patterning system that apparently keeps gnathostome jaws in functional registration yet tractable to potential changes in functional demands over time. It relies upon a system for the establishment of positional information where pattern and placement of the "hinge" is driven by factors common to the junction of the maxillary and mandibular branches of the first arch and of the "caps" by the signals emanating from the distal-most first arch midline and the lamboidal junction (where the maxillary branch meets the frontonasal processes). In this particular model, the functional registration of jaws is achieved by the integration of "hinge" and "caps" signaling, with the "caps" sharing at some critical level a developmental history that potentiates their own coordination. We examine the evidential foundation for this model in mice, examine the robustness with which it can be applied to other taxa, and examine potential proximate sources of the signaling centers. Lastly, as developmental biologists have long held that the anterior-most mesendoderm (anterior archenteron roof or prechordal plate) is in some way integral to the normal formation of the head, including the cranial skeletal midlines, we review evidence that the seminal patterning influences on the early anterior ectoderm extend well beyond the neural plate and are just as importan...

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Section: Figmentioning

confidence: 99%

21^st Century neontology and the comparative development of the vertebrate skull

Depew

Simpson

2006

Developmental Dynamics

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“…Indeed Edn1 is expressed in the endoderm and in the mesodermal core of the mandibular prominence of PA1, whereas Ednra (Edn1 receptor-type A) is broadly expressed by the CNCC-derived PA1 ectomesenchyme and Dlx5;Dlx6 are only expressed in the mesenchyme of the mandibular prominence (Abe et al, 2007;Clouthier et al, 1998Clouthier et al, , 2000Ozeki et al, 2004;Ruest et al, 2004Ruest et al, , 2005. Loss of Edn1?Ednra signaling results in the down regulation of the two members of the distalless homeobox gene family Dlx5 and Dlx6 (Merlo et al, 2002a;Panganiban and Rubenstein, 2002), and in a homeotic-like transformation of lower into upper jaw structures, similar to that observed upon double inactivation of Dlx5 and Dlx6 (Beverdam et al, 2002;Depew et al, 2002;Fukuhara et al, 2004;Ruest et al, 2004). The constitutive activation of the Edn1?Ednra signaling in the entire PA1 induces a partial transformation of the upper jaw suggesting that PA1 CNCCs are competent to respond to Edn1 signaling.…”

Section: Introductionmentioning

confidence: 99%

Spatio‐temporal dynamics of gene expression of the Edn1‐Dlx5/6 pathway during development of the lower jaw

Vieux-Rochas

Mantero

Heude

et al. 2010

Genesis

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Summary: The morphogenesis of the vertebrate skull results from highly dynamic integrated processes involving the exchange of signals between the ectoderm, the endoderm, and cephalic neural crest cells (CNCCs). Before migration CNCCs are not committed to form any specific skull element, molecular signals exchanged in restricted regions of tissue interaction are crucial in providing positional identity to the CNCCs mesenchyme and activate the specific morphogenetic process of different skeletal components of the head. In particular, the endothelin-1 (Edn1)-dependent activation of Dlx5 and Dlx6 in CNCCs that colonize the first pharyngeal arch (PA1) is necessary and sufficient to specify maxillo-mandibular identity. Here, to better analyze the spatio-temporal dynamics of this process, we associate quantitative gene expression analysis with detailed examination of skeletal phenotypes resulting from combined allelic reduction of Edn1, Dlx5, and Dlx6. We show that Edn1-dependent and -independent regulatory pathways act at different developmental times in distinct regions of PA1. The Edn1?Dlx5/6?Hand2 pathway is already active at E9.5 during early stages of CNCCs colonization. At later stages (E10.5) the scenario is more complex: we propose a model in which PA1 is subdivided into four adjacent territories in which distinct regulations are taking place. This new developmental model may provide a conceptual framework to interpret the craniofacial malformations present in several mouse mutants and in human first arch syndromes. More in general, our findings emphasize the importance of quantitative gene expression in the fine control of morphogenetic events. genesis 48:362-373, 2010.

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“…One of the main aims of our study was to identify genes that could be used as markers of the different facial prominences. There are an increasing number of studies where genetic or molecular manipulations have resulted in dramatic homeotic transformations of the jaws (Miller et al, 2000;Lee et al, 2001;Kimmel et al, 2003Kimmel et al, , 2007Ruest et al, 2004;Sato et al, 2008). One difficulty in determining whether the molecular landscape of the transformed region is converted to the new identity is that it is difficult to find genes that are restricted to different regions of the face.…”

Section: Discussionmentioning

confidence: 99%

“…However, other targeting experiments in which the first branchial arch enhancer of Hand2 was selectively deleted showed major reductions in the mandible (Yanagisawa et al, 2003). Hand2 is in the pathway that controls mandibular identity (Depew et al, 2002;Ruest et al, 2004), but no changes in identity were observed in the enhancer knockout. Studies that investigate genetic interactions between Hand2 and Dlx5/6 or Ednra (Endothelin receptor A) may yet reveal a contributing role for Hand2 in specifying identity.…”

Section: Genes That Characterize the Mandibular Prominencesmentioning

confidence: 93%

“…These later expressed genes include those essential for patterning of the mesenchyme such as Distaless related genes Dlx5/6 (Distaless homeobox; Beverdam et al, 2002;Depew et al, 2002) and the upstream signal Edn1 (Endothelin1; Ozeki et al, 2004) or its receptor Endra1 (Ruest et al, 2004). These loss-offunction experiments highlight the fact that genes expressed in the neural crest-derived facial mesenchyme are necessary for large scale jaw patterning.…”

Section: Introductionmentioning

confidence: 99%

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Whole genome microarray analysis of chicken embryo facial prominences

Buchtová

Kuo

Nimmagadda

et al. 2010

Developmental Dynamics

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The face is one of the three regions most frequently affected by congenital defects in humans. To understand the molecular mechanisms involved, it is necessary to have a more complete picture of gene expression in the embryo. Here, we use microarrays to profile expression in chicken facial prominences, post neural crest migration and before differentiation of mesenchymal cells. Chip-wide analysis revealed that maxillary and mandibular prominences had similar expression profiles while the frontonasal mass chips were distinct. Of the 3094 genes that were differentially expressed in one or more regions of the face, a group of 56 genes was subsequently validated with quantitative polymerase chain reaction (QPCR) and a subset examined with in situ hybridization. Microarrays trends were consistent with the QPCR data for the majority of genes (81%). On the basis of QPCR and microarray data, groups of genes that characterize each of the facial prominences can be determined. Developmental Dynamics 239:574-591,

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Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity

Cited by 138 publications

References 71 publications

21^st Century neontology and the comparative development of the vertebrate skull

21^st Century neontology and the comparative development of the vertebrate skull

Spatio‐temporal dynamics of gene expression of the Edn1‐Dlx5/6 pathway during development of the lower jaw

Whole genome microarray analysis of chicken embryo facial prominences

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Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity

Cited by 138 publications

References 71 publications

21st Century neontology and the comparative development of the vertebrate skull

21st Century neontology and the comparative development of the vertebrate skull

Spatio‐temporal dynamics of gene expression of the Edn1‐Dlx5/6 pathway during development of the lower jaw

Whole genome microarray analysis of chicken embryo facial prominences

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21^st Century neontology and the comparative development of the vertebrate skull

21^st Century neontology and the comparative development of the vertebrate skull