Formation of a “Pre-mouth Array” from the Extreme Anterior Domain Is Directed by Neural Crest and Wnt/PCP Signaling

Jacox, Laura Anne; Chen, Justin; Rothman, Alyssa; Lathrop-Marshall, Hillary; Sive, Hazel

doi:10.1016/j.celrep.2016.06.073

Cited by 16 publications

(30 citation statements)

References 37 publications

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“…Concentrations ranging from 50 to 100 µm were effective in causing a persistent buccopharyngeal membrane when the media and inhibitor were refreshed one time at stage 39. Earlier treatments also resulted in embryonic mouth defects, but these may be due to JNK's role in other processes during orofacial development (Jacox et al, ) and are not shown.…”

Section: Resultsmentioning

confidence: 97%

Role of JNK during buccopharyngeal membrane perforation, the last step of embryonic mouth formation

Houssin

Bharathan

Turner

et al. 2016

Developmental Dynamics

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Background The buccopharyngeal membrane is a thin layer of cells covering the embryonic mouth. The perforation of this structure creates an opening connecting the external and the digestive tube which is essential for oral cavity formation. In humans, persistence of the buccopharyngeal membrane can lead to orofacial defects such as choanal atresia, oral synechiaes and cleft palate. Little is known about the causes of a persistent buccopharyngeal membrane and importantly how this structure ruptures. Results We have determined that Xenopus embryos deficient JNK signaling, using antisense and pharmacological approaches, have a persistent buccopharyngeal membrane. JNK deficient embryos have decreased cell division and increased cellular stress and apoptosis. However, altering these processes independently of JNK did not affect buccopharyngeal membrane perforation. JNK deficient embryos also have increased intercellular adhesion and defects in e-cadherin localization. Conversely, embryos with overactive JNK have epidermal fragility, increased E-cadherin internalization and increased membrane localized clathrin. In the buccopharyngeal membrane, clathrin is colocalized with active JNK. Further, inhibition of endocytosis results in a persistent buccopharyngeal membrane, mimicking the JNK deficient phenotype. Conclusions The results of this study suggest that JNK has a role in the disassembly adherens junctions via endocytosis that is required during buccopharyngeal membrane perforation.

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Section: Resultsmentioning

confidence: 97%

Role of JNK during buccopharyngeal membrane perforation, the last step of embryonic mouth formation

Houssin

Bharathan

Turner

et al. 2016

Developmental Dynamics

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“…In sea urchins and basal deuterostomes that lack a central nervous system or brain, mouth ectoderm arises from the epidermal layers . In vertebrates, oral ectoderm derives also from the anterior neural ridge (ANR), the front of the neural plate . This dual source of mouth ectoderm is also found in Ciona, an invertebrate chordate, whose mouth is derived from the anterior neuropore .…”

Section: Oral Evolution: Is Mouth Development Conserved?mentioning

confidence: 99%

“…This is EAD ectoderm that will surround the mouth opening and contribute to the oral cavity. Subsequently, a basement membrane forms that separates the developing brain from EAD ectoderm . Overlying epidermal ectoderm can be substituted by flank epidermal ectoderm and is therefore not specific for mouth development .…”

Section: Steps To Form a Mouth: Xenopus As A Paradigmmentioning

confidence: 99%

“…Interestingly, even in triploblastic animals that include mesoderm, the mouth still forms from a region where ectoderm and endoderm directly juxtapose . In chordates, we named this region the extreme anterior domain (EAD) . Another aspect of the ancient origin of the mouth is conservation of gene expression, leading to the proposal of a ‘mouth gene program.’…”

Section: Introductionmentioning

confidence: 99%

“…Vertebrates are ‘deuterostomes’ where a mouth breaks through the ectodermal covering and connects to the endodermal digestive tract. In the Xenopus model, development of the vertebrate mouth is associated with reciprocal signaling between the EAD and NC . Mouth formation reflects this precision and involves many steps over a long period of development (~2.5 days in Xenopus , 2 weeks in humans).…”

Section: Introductionmentioning

confidence: 99%

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Mouth development

Chen

Jacox

Saldanha

et al. 2017

WIREs Developmental Biology

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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.275For further resources related to this article, please visit the WIREs website.

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Models of convergent extension during morphogenesis

Shindo

2017

WIREs Developmental Biology

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Convergent extension (CE) is a fundamental and conserved collective cell movement that forms elongated tissues during embryonic development. Thus far, studies have demonstrated two different mechanistic models of collective cell movements during CE. The first, termed the crawling mode, was discovered in the process of notochord formation in Xenopus laevis embryos, and has been the established model of CE for decades. The second model, known as the contraction mode, was originally reported in studies of germband extension in Drosophila melanogaster embryos and was recently demonstrated to be a conserved mechanism of CE among tissues and stages of development across species. This review summarizes the two modes of CE by focusing on the differences in cytoskeletal behaviors and relative expression of cell adhesion molecules. The upstream molecules regulating these machineries are also discussed. There are abundant studies of notochord formation in X. laevis embryos, as this was one of the pioneering model systems in this field. Therefore, the present review discusses these findings as an approach to the fundamental biological question of collective cell regulation. WIREs Dev Biol 2018, 7:e293. doi: 10.1002/wdev.293This article is categorized under: Early Embryonic Development > Gastrulation and NeurulationComparative Development and Evolution > Model Systems

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Formation of a “Pre-mouth Array” from the Extreme Anterior Domain Is Directed by Neural Crest and Wnt/PCP Signaling

Cited by 16 publications

References 37 publications

Role of JNK during buccopharyngeal membrane perforation, the last step of embryonic mouth formation

Role of JNK during buccopharyngeal membrane perforation, the last step of embryonic mouth formation

Mouth development

Models of convergent extension during morphogenesis

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