Abstract

Pharyngeal endoderm is essential for and can reprogram development of the head skeleton. Here we investigate the roles of specific endodermal structures in regulating craniofacial development. We have isolated an integrinα5 mutant in zebrafish that has region-specific losses of facial cartilages derived from hyoid neural crest cells. In addition, the cranial muscles that normally attach to the affected cartilage region and their associated nerve are secondarily reduced in integrinα5− animals. Earlier in development, integrinα5 mutants also have specific defects in the formation of the first pouch, an outpocketing of the pharyngeal endoderm. By fate mapping, we show that the cartilage regions that are lost in integrinα5 mutants develop from neural crest cells directly adjacent to the first pouch in wild-type animals. Furthermore, we demonstrate that Integrinα5 functions in the endoderm to control pouch formation and cartilage development. Time-lapse recordings suggest that the first pouch promotes region-specific cartilage development by regulating the local compaction and survival of skeletogenic neural crest cells. Thus, our results reveal a hierarchy of tissue interactions, at the top of which is the first endodermal pouch, which locally coordinates the development of multiple tissues in a specific region of the vertebrate face. Lastly, we discuss the implications of a mosaic assembly of the facial skeleton for the evolution of ray-finned fish.

Highlights

  • The skeletal elements that form and support the vertebrate jaw and gills are derived from a specialized population of ectomesenchyme cells, the cranial neural crest (Platt 1893; Le Douarin 1982; Schilling and Kimmel 1994; but see Weston et al 2004)

  • We found that the regions of the HS cartilage that are lost in integrina5 mutants develop from anterior crest–derived cells immediately adjacent to the first pouch

  • We confirmed by reverse transcription polymerase chain reaction (RT-PCR) that itga5-MO effectively inhibits the splicing of integrina5 (Figure 1E and 1F)

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Summary

Introduction

The skeletal elements that form and support the vertebrate jaw and gills are derived from a specialized population of ectomesenchyme cells, the cranial neural crest (Platt 1893; Le Douarin 1982; Schilling and Kimmel 1994; but see Weston et al 2004). Crest cells of the first, or mandibular, arch give rise to Meckel’s and palatoquadrate cartilages that constitute the lower and upper jaws, respectively. Several cartilages are derived from the second, or hyoid, arch, including the ceratohyal (CH) and hyosymplectic (HS) cartilages that support the jaw. The HS cartilage serves to connect the upper jaw to the skull by means of a hyomandibula (HM) plate and a symplectic (SY) anterior rod-like extension.

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