Endodermal/ectodermal interfaces during pharyngeal segmentation in vertebrates

Abstract

A key event in the formation of the pharyngeal arches is the outpocketing of the endodermal pharyngeal pouches and the establishment of contact with the overlying ectoderm. However, relatively little is known about how the endoderm and ectoderm relate to each other at these points of contact and the extent to which this differs between the pouches. We have therefore detailed the interactions between the pharyngeal pouches and ectoderm in the chick embryo. Unlike the other pouches, the first pouch does not sustain direct contact with the ectoderm but separates after initial contact. Contrastingly, a perforation is formed between the second pouch and cleft that creates an external opening into the pharynx. Finally, the third and fourth pouch endoderm can be seen to bulge outwards through the ectoderm, although external openings to the pharyngeal lumen are not established. To understand whether these behaviours represent derived or ancestral features, we characterised the pharyngeal ectodermal-endodermal interfaces in the shark embryo. We found that the pouches of the posterior gill-bearing arches in this species also displayed the outward bulging of the endoderm into the ectoderm, although openings were established. We further used genetic tools to detail unambiguously the relationship between the endoderm and ectoderm in zebrafish and mouse embryos and again found that the posterior pouches break through the ectoderm. Thus different pharyngeal pouches establish different topological relationships with the overlying ectoderm and the posterior pouches initiate the developmental programme for the formation of gills, be they amniotes or anamniotes.

Tbx1 and Foxi3 genetically interact in the third pharyngeal pouch endoderm required for thymus and parathyroid development

“…Rather, the ectoderm can initiate invagination independently. This is consistent with studies done in shark and chick embryos where the endoderm remains separate from the ectoderm throughout epithelial cell invagination (Shone and Graham, 2014).…”

“…During vertebrate embryonic development, the segmentation of the PA is needed to create individual arches that later form derivative structures including the thymus and parathyroid glands (Graham et al, 2005;Shone and Graham, 2014). We revisited the process of pharyngeal segmentation to better understand the functions of Tbx1 and Foxi3.…”

“…While the formation of PA1 is normal, PA2 is hypoplastic or absent, and the distal pharyngeal arches, PA3-6 do not form (Jerome and Papaioannou, 2001;Lindsay et al, 2001;Merscher et al, 2001). Since the PE is critically important for segmentation of the distal PA (Quinlan et al, 2004;Shone and Graham, 2014), it is important to understand the genes and processes that might act downstream.…”

The Origin of Vertebrate Gills

“…Pharyngeal arch development begins with the iterative outpocketing of foregut endoderm in a rostral-to-caudal sequence, giving rise to a series of endodermal pouches [16]. These pouches subsequently contact and fuse with overlying surface ectoderm, resulting in the perforation of gill slits and the delineation of arches (Figure 2A).…”

Neural crest and the origin of species‐specific pattern

“…Such a conclusion is further supported by experiments that alter combinatorial codes of transcription factors including the Dlx genes, and that genetically manipulate signaling pathways such as endothelin , which affect the axial pattern, outgrowth, and in some instances switch the anatomical identify of the maxillary and the mandibular primordia (Depew et al, ; Kuraku, Takio, Sugahara, Takechi, & Kuratani, ; Miller, Yelon, Stainier, & Kimmel, ; Sato et al, ; Tavares et al, ; Tavares et al, ). Notably, these molecular mechanisms and gene regulatory networks that pattern the axes and impart anatomical identity within the pharyngeal arches and other regions of the craniofacial complex have remained highly conserved across vertebrates (Cerny, Lwigale, et al, ; Cerny, Meulemans, et al, ; Depew & Compagnucci, ; Kuraku et al, ; Kuratani, ; Kuratani, Adachi, Wada, Oisi, & Sugahara, ; Kuratani, Nobusada, Horigome, & Shigetani, ; Kuratani, Oisi, & Ota, ; Medeiros & Crump, ; Minarik et al, ; Myojin et al, ; Nikitina, Sauka‐Spengler, & Bronner‐Fraser, ; Oisi, Ota, Fujimoto, & Kuratani, ; Oisi, Ota, Kuraku, Fujimoto, & Kuratani, ; Olsson, Ericsson, & Cerny, ; Ota, Kuraku, & Kuratani, ; Sauka‐Spengler, Meulemans, Jones, & Bronner‐Fraser, ; Shigetani et al, ; Shone & Graham, ; Square, Jandzik, Romasek, Cerny, & Medeiros, ; Sugahara et al, ; Takio et al, ; Yao, Ohtani, Kuratani, & Wada, ). This level of conservation indicates that all vertebrates more or less deploy the same gene regulatory networks, signaling pathways, and developmental modules to specify their axes and determine the anatomical identity of the homologous structures from which their craniofacial complexes get built.…”