Chen J et al. (2017), Mouth development. - ???displayArticle.title???

XB-ART-53697

Wiley Interdiscip Rev Dev Biol 2017 Sep 01;65:. doi: 10.1002/wdev.275.

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Mouth development.

Chen J , Jacox LA , Saldanha F , Sive H .

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A mouth is present in all animals, and comprises an opening from the outside into the oral cavity and the beginnings of the digestive tract to allow eating. This review focuses on the earliest steps in mouth formation. In the first half, we conclude that the mouth arose once during evolution. In all animals, the mouth forms from ectoderm and endoderm. A direct association of oral ectoderm and digestive endoderm is present even in triploblastic animals, and in chordates, this region is known as the extreme anterior domain (EAD). Further support for a single origin of the mouth is a conserved set of genes that form a 'mouth gene program' including foxA and otx2. In the second half of this review, we discuss steps involved in vertebrate mouth formation, using the frog Xenopus as a model. The vertebrate mouth derives from oral ectoderm from the anterior neural ridge, pharyngeal endoderm and cranial neural crest (NC). Vertebrates form a mouth by breaking through the body covering in a precise sequence including specification of EAD ectoderm and endoderm as well as NC, formation of a 'pre-mouth array,' basement membrane dissolution, stomodeum formation, and buccopharyngeal membrane perforation. In Xenopus, the EAD is also a craniofacial organizer that guides NC, while reciprocally, the NC signals to the EAD to elicit its morphogenesis into a pre-mouth array. Human mouth anomalies are prevalent and are affected by genetic and environmental factors, with understanding guided in part by use of animal models. WIREs Dev Biol 2017, 6:e275. doi: 10.1002/wdev.275 For further resources related to this article, please visit the WIREs website.

???displayArticle.pubmedLink??? 28514120
???displayArticle.pmcLink??? PMC5574021
???displayArticle.link??? Wiley Interdiscip Rev Dev Biol
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Species referenced: Xenopus laevis
Genes referenced: aldh1a2 cpn1 fgf8 frzb hesx1 otx2 pitx2 pitx3 prdm1 shh tbxt
GO keywords: gut morphogenesis [+]

???displayArticle.disOnts??? Nager acrofacial dysostosis
???displayArticle.omims??? ACROFACIAL DYSOSTOSIS 1, NAGER TYPE; AFD1 [+]

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	Figure 1. Mouths in adult or larval animals. Frontal views of sea anemone Anthopleura elegantissima, earth worm Lumbricus terrestris, sea urchin Strongylocentrotus purpuratus, grasshopper Anacridium aegyptium, lamprey Petromyzon marinus, tadpole of frog Xenopus laevis, falcon Falco cherrug, and human Homo sapiens. Red dotted line denotes the border of the oral cavity. Md, mandible; Mx, maxilla; P, pharynx; T, teeth; Tg, tongue.
	Figure 2. Mouth forms where ectoderm and endoderm are juxtaposed. (a) Position of future mouth relative to germ layers in embryos of three representative animals. Schematics of sagittal sections are shown for the diploblast cnidarian Nematostella vectensis (invertebrate), the triploblasts and deuterostomes sea urchin Strongylocentrotus purpuratus (invertebrate) and frog Xenopus laevis (vertebrate). The red box outlines the mouth-forming region made up of juxtaposed ectoderm and endoderm. In vertebrates, this region is termed the extreme anterior domain. (b) Ancestral mouth embryonic gene expression domains in N. vectensis, S. purpuratus, and X. laevis (purple). The mouth expression domain of foxA and otx but not brachyury is conserved in vertebrates.
	Figure 3. Ancestral mouth was present in the common ancestor of cnidaria and triploblasts. (a) Phylogenetic tree. Chordates, echinoderms, and cnidaria are three distantly related phyla that retain common mouth characteristics, suggesting that the mouth evolved once. (b) Criteria used to evaluate mouth evolution. The mouths of cnidaria, echinoderms, and chordates are all comprised of ectoderm and endoderm and express foxA and otx. There are phylum-specific characteristics such as neural ectoderm contributing to the chordate mouth and the expression of blimp1, gataE , and pitx in echinoderm and chordates. Analysis of axial positioning genes demonstrates that the cnidarian oral–aboral axis is equivalent to the echinoderm and chordate posterior–anterior axis.
	Figure 4. Relationship of the extreme anterior domain (EAD) and neural crest (NC) to the Xenopus mouth. Branchial arch (BA, light green) NC, and frontonasal prominence crest (FNP, dark green) delaminate from the dorsal neural tube (NT) at neurula. The EAD (red outline) is specified including cells arising from the anterior neural ridge (ANR, black outline) and cement gland (CG, brown) tissue. The EAD (purple) will contribute to the lining of the mouth (as well as the nostrils and anterior pituitary). FNP NC migrates anteriorly between the eyes to enter the face while first BA NC migrates bilaterally into the face (late neural-mid tailbud). Subsequent to NC ingress, EAD ectoderm thins and lengthens to become the ‘pre-mouth array’ (early-mid tailbud). NC cells eventually differentiate to form the facial skeleton, including the palate, maxilla, mandible, and connective tissue.
	Figure 5. Extreme anterior domain (EAD) gene expression domains in Xenopus. Frontal views of Xenopus tadpole embryos. Selected gene expression domains are shown that include the EAD. These include pitx1c, pitx2, pitx3, vgl2, xanf1, cpn, frzb1, shh, fgf8, and raldh2. See text for details on their function in mouth development.
	Figure 6. Steps in Xenopus mouth formation. (a) Coronal views of steps to mouth opening. Frontal views of the embryo are shown. The extreme anterior domain (EAD) begins at early tailbud (st. 22) as a wide, short block of cells. By late tailbud (st. 28), the neural crest (NC) migrates to lie on either side of the EAD. Signals from the NC initiate convergent extension in the EAD so that it forms a pre-mouth array. Apico-basal polarity is established in the pre-mouth array, which separates down the midline to form the stomodeum at hatching stages (st. 35/36), that opens into the mouth at tadpole stage (st. 40). NC is in light green. (b) Sagittal views of steps to mouth opening. The EAD from a tailbud embryo showing different germ layers is enlarged in schematics below. Epidermal ectoderm is not shown in enlarged schematics. At late tailbud (st. 28), the pre-mouth array forms by convergent extension, and the basement membrane (BM) between EAD ectoderm and endoderm disintegrates. The pre-mouth array opens to form the stomodeal invagination. Stomodeal ectoderm thins concurrent with a burst of apoptosis and migration of ectoderm out of the region at hatching stages (st. 34–37). Intercalation of ectoderm and endoderm produces the buccopharyngeal membrane (BPM), which perforates to open the mouth at tadpole stages (st. 39–40).
	Figure 7. Reciprocal signaling between extreme anterior domain (EAD) organizer and cranial neural crest (NC). The EAD secretes signals, including Kinin peptides, that guide the NC into the face. As they migrate into the face, NC cells secrete factors including Wnt/PCP ligands that stimulate EAD convergent extension to form the ‘pre-mouth array.’ The pre-mouth array later opens down the midline to form the stomodeum and edges of the future mouth.

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