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WIREs Dev Biol
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Development and evolution of the pharyngeal apparatus

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The oral or pharyngeal apparatus facilitates the dual functions of respiration and feeding. It develops during embryogenesis from transient structures called pharyngeal arches (PAs), which comprise a reiterated series of outgrowths on the lateral side of the head. The PAs and their segmental arrangement are highly conserved throughout evolution from invertebrate chordates such as amphioxus, through to vertebrate agnathans including avians, squamates, and mammals. The structural organization of the PAs is also highly conserved and involves contributions from each of the three primary endoderm, mesoderm, and ectoderm germ layers. The endoderm is particularly important for PA formation and segmentation and also plays a critical role in tissue‐specific differentiation. The ectoderm gives rise to neural crest cells (NCC) which provide an additional layer of complexity to PA development and differentiation in vertebrates compared to invertebrate chordates that do not possess NCC. Collectively, the PAs give rise to much of the neurovasculature and musculoskeletal systems in the head and neck. The complexity of development renders the pharyngeal apparatus prone to perturbation and subsequently the pathogenesis of birth defects. Hence it is important to understand the signals and mechanisms that govern the development and evolution of the pharyngeal complex. WIREs Dev Biol 2014, 3:403–418. doi: 10.1002/wdev.147 This article is categorized under: Early Embryonic Development > Development to the Basic Body Plan Vertebrate Organogenesis > Musculoskeletal and Vascular Nervous System Development > Vertebrates: Regional Development
Structural organization of the pharyngeal arches in a human embryo. Schematic illustration of the internal organization of the developing pharyngeal arches (PAs). Each PA is numbered from 1 to 6. PAs are lined externally by ectoderm in pink and internally by endoderm in purple. Inside, each PA is a mesenchymal core (blue) composed of mesoderm cells surrounded by NCC cells alongside the nerve (yellow) and blood vessel (red) components.
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Dlx and Hox gene control of pharyngeal patterning. Dapi staining of E10.5 mouse embryo. Expression domain of Dlx1 and Dlx2 (yellow) in the first and second pharyngeal arch (PA). Nested expression of Dlx5 and Dlx6 (orange) within the Dlx1 and Dlx2 domains of expression. Hox2 group genes are expressed in the second PA (pink) and more posterior Pas, while Hox group 3 (blue) and Hox group 4 (green) genes are expressed in the third and fourth PAs respectively.
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Evolutionary cladogram. Evolutionary tree showing the classification of species from deuterostomes to mammals. Neural crest cells (NCCs) appear during the transition to vertebrates.
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Pharyngeal arch vascular patterning. The maxillary artery (green) is derived from the first pharyngeal arch artery (PAA). The stapedial (red) is derived from the second PAA. The carotid system (purple) derives from the third PAA. The left fourth PAA gives rise to the aortic arch while the right PAA gives rise to the subclavian artery and contributes to the pulmonary arteries (light blue). Finally, the sixth PAA gives rise to the ductus arteriosus (dark blue).
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Establishment of the musculature, vasculature, and PNS of the face in mouse embryo. (a) LacZ staining marking NCC. (b) tbx1 in situ hybridization showing the myogenic core of each PA. (c) PECAM immunostaining marking endothelial cells of the developing vasculature. (d) TUJ1 immunostaining marking NCC and placode‐derived neurons. (e) Eya2 in situ hybridization, delimiting the cranial placodes.
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Pharyngeal arch differentiation. (a) Schematic illustration of the pharyngeal region of a human embryo. (b) Skeletal derivatives of the NCC. Bones of the face are formed by two ossification processes. Endochondral bones are formed via a cartilage template and include the maleus (from Meckel's cartilage), and the incus (from maxillary cartilage) from the first PA (green). The stapes, the styloid process and lesser horn of hyoid (from Reichter's cartilage) come from the second PA (red). Dermal bone formation consists of direct ossification of the NCC without a cartilage intermediate. Dermal elements include the squamous part of the temporal bone, the zygomatic, the maxillary bone and the mandible, which are derived from first PA (green). (c) Neural derivatives of the NCC. The trigeminal nerve (V) comprises three subdivisions: the ophthalmic nerve, the maxillary nerve, and the mandibular nerve and develops in association with the first PA, (green). The facial nerve invades the second PA (red). The glossopharyngeal invades the third PA (purple) and the vagus nerve the fourth PA (dark blue). (d) Muscular derivatives of the mesoderm. Muscles (green) of mastication are derived from mesoderm of the first PA. Muscles of facial expression (red) are derived from second PA mesoderm. The stylopharyngeus (purple) is the only muscle that is derived from the third PA mesoderm. The external muscles of the pharynx (blue) are derived from fourth PA mesoderm.
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Vertebrate Organogenesis > Musculoskeletal and Vascular
Nervous System Development > Vertebrates: Regional Development
Early Embryonic Development > Development to the Basic Body Plan