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Dual Origins of the Prechordal Cranium in the Chicken Embryo

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Dual Origins of the Prechordal Cranium in the Chicken Embryo Developmental Biology 356 (2011) 529–540 Contents lists available at ScienceDirect Developmental Biology journal homepage: www.elsevier.com/developmentalbiology Dual origins of the prechordal cranium in the chicken embryo Naoyuki Wada a,⁎, Tsutomu Nohno a, Shigeru Kuratani b a Molecular and Developmental Biology, Kawasaki Medical School, 577 Matsushima, Kurashiki, 701–0192, Japan b Laboratory for Evolutionary Morphology, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-minami, Chuo, Kobe, Hyogo 650-0047, Japan article info abstract Article history: The prechordal cranium, or the anterior half of the neurocranial base, is a key structure for understanding the Received for publication 30 April 2010 development and evolution of the vertebrate cranium, but its embryonic configuration is not well understood. Revised 1 May 2011 It arises initially as a pair of cartilaginous rods, the trabeculae, which have been thought to fuse later into a Accepted 6 June 2011 single central stem called the trabecula communis (TC). Involvement of another element, the intertrabecula, Available online 14 June 2011 has also been suggested to occur rostral to the trabecular rods and form the medial region of the prechordal cranium. Here, we examined the origin of the avian prechordal cranium, especially the TC, by observing the Keywords: Prechordal cranium craniogenic and precraniogenic stages of chicken embryos using molecular markers, and by focal labeling of Trabecula the ectomesenchyme forming the prechordal cranium. Subsequent to formation of the paired trabeculae, a Intertrabecula cartilaginous mass appeared at the midline to connect their anterior ends. During this midline cartilage Neural crest cells formation, we did not observe any progressive medial expansion of the trabeculae. The cartilages consisted of Fate mapping premandibular ectomesenchyme derived from the cranial neural crest. This was further divided anteroposteriorly into two portions, derived from two neural crest cell streams rostral and caudal to the optic vesicle, called preoptic and postoptic neural crest cells, respectively. Fate-mapping analysis elucidated that the postoptic neural crest cells were distributed exclusively in the lateroposterior part of the prechordal cranium corresponding to the trabeculae, whereas the preoptic stream of cells occupied the middle anterior part, differentiating into a cartilage mass corresponding to the intertrabecula. These results suggest that the central stem of the prechordal cranium of gnathostomes is composed of two kinds of distinct cartilaginous modules: a pair of trabeculae and a median intertrabecula, each derived from neural crest cells populating distinct places of the craniofacial primordia through specific migratory pathways. © 2011 Elsevier Inc. All rights reserved. Introduction (Couly et al., 1993). The central stem of the prechordal cranium corresponds to the main portion of the ethmosphenoidal region, or the The vertebrate neurocranium represents a major component of the chondrocranial component preformed by a pair of trabeculae, which cranium. It has been regarded traditionally either as a cartilaginous bowl develop on both sides of Rathke's pouch and the internal carotid arteries with a series of fenestrae for cranial nerves, or as composed of a central (Couly et al., 1993; de Beer, 1937; Goodrich, 1930; Kuratani et al., 1997; stem associated with paired pillar-like structures—often compared with McBratney-Owen et al., 2008). Subsequently, the trabeculae are thought neural arches in the trunk—as well as some sensory capsules such as the to fuse at the midline to form a single median element: the trabecula nasal and otic capsules (de Beer, 1937; Gaupp, 1906; Goodrich, 1930; communis (TC) (de Beer, 1937; Fig. 1A). Starck, 1979). The basal part arises primarily as two pairs of cartilaginous In nonmammalian amniotes, the TC is a direct precursor for the rods: the trabeculae anteriorly and the parachordals posteriorly. interorbital septum posteriorly and the nasal septum (NS) anteriorly Developmentally, the neurocranium is known now to originate from (Figs. 1A and 2D–D’). Morphogenesis of the embryonic avian cranium two distinct cell lineages: the cephalic crest cells and the head mesoderm has been reported for over a century by various authors and the (Couly et al., 1993; McBratney-Owen et al., 2008). That part of the morphogenetic pattern of the prechordal cranium has been described neurocranium rostral to the notochord is called the prechordal cranium (Bellairs, 1958; de Beer, 1937; Parker, 1890; Suschkin, 1899; Vorster, and is derived exclusively from the cranial neural crest, unlike the 1989). Despite ample histological observations, there remain contro- posterior or chordal cranium that is derived from the head mesoderm versies as to the developmental origins and initial development of the TC, even in the chicken embryo, as discussed in Vorster (1989). Of the remaining questions, the most fundamental concerns the precursors for the prechordal cranium. Several authors have proposed ⁎ Corresponding author at: Applied Biological Science, Faculty of Science and that this element, especially the TC, is composed of two distinct Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510, Japan. Fax: +81 4 7123 9767. cartilaginous primordia: the lateroposterior and the medioanterior. The E-mail address: [email protected] (N. Wada). former corresponds to the direct derivative of the paired trabeculae, 0012-1606/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ydbio.2011.06.008 530 N. Wada et al. / Developmental Biology 356 (2011) 529–540 specified not at the premigratory stage along the anteroposterior (AP) axis of the crest origin, but at the postmigratory stage of neural crest cells, which populate locations corresponding to specific anatomical patterns of the prechordal cranial primordia. Materials and methods Embryos White Leghorn chicken eggs were incubated at 38 °C and embryos were staged according to Hamburger and Hamilton (1951; defined as HH stages below). Quail embryos were staged similarly, mainly based on the numbers of somites and embryonic head morphology. Orthotopic transplantation of neural crest cells Orthotopic transplantation of neural crest cells was performed as follows. Chicken embryos at the 8–9 somite stage were used as hosts and quail embryos of equivalent developmental stages served as donors. A small rectangular region consisting of the ectoderm and underlying neural crest cells of the dorsal neural tube was removed from the chicken host and a fragment excised from the same region of Fig. 1. (A) Development of the trabecular cartilage. Cartilaginous elements derived from a quail embryo was implanted into the gap of the host with correct cranial neural crest cells are shown in blue. A pair of cartilaginous bars, the trabeculae, is orientation (see Figs. 6A and 7A). After this transplantation, the formed lateral to Rathke's pouch (Rp, left) and then fuses at the midline to form a single embryos were reincubated up to HH stages 28–30 to be prepared for median stem, the trabecula communis (TC, right). This forms the interorbital cartilage posteriorly and the nasal septum anteriorly. NC, nasal capsule; OV, optic vesicle. immunohistochemical analysis as described below. (B) Models of trabecular formation. (a) A classical model. Cells in the trabecular cartilage grow medially (red arrows) and fuse at the midline. (b) Another model. In Fluorescent dye labeling addition to the paired trabeculae, another intermediate cartilaginous aggregate (ITC) is formed between and anterior to the paired trabeculae and these three elements fuse. Fluorescent dye labeling of cranial neural crest cells was performed on chicken embryos at 8–10 somite stages. DiI (Invitrogen) was dissolved in 100% ethanol at 2 mg/ml and then diluted 1/10 with whereas the latter, called the ‘intertrabecular cartilage’, was thought to 0.3% sucrose solution. To observe the migratory direction of the crest – be formed between and rostral to the paired trabeculae, forming the cells near the diencephalon mesencephalon boundary, the DiI midline septum (Fig. 1B). solution was injected focally onto a subset of neural crest cells near The existence of a cellular aggregate for the intertrabecula was the boundary, based on the result of human natural killer-1 (HNK-1) suggested, for example, in a kestrel embryo (Suschkin, 1899;reviewed immunostaining (see below; Fig. 4). The embryos were allowed to fi by de Beer, 1937). Bellairs (1958) reported that the intertrabecular develop, xed after 24 h and observed for the distribution of the mesenchyme intervenes with the paired trabecular rods and later fuses labeled cells. For analyzing the fate of neural crest cells in the with the latter to form a median cartilage. However, the presence of the prechordal cranium, we labeled the subsets of either migratory intertrabecular mesenchyme has been refuted by some other authors, preoptic or postoptic crest cells and left the embryos to develop up to – fi including de Beer (1937). He questioned whether it really forms as a HH stages 27 28, when they were xed for immunohistochemistry. distinct element independent from the trabecula. Vorster (1989) concluded that at least the ‘cartilaginous intertrabecula’ is not found Immunohistochemistry in the early prechordal cranium and that it merely represents a region of fewer intercellular matrices at later stages. These different opinions Chicken embryos were placed in Bouin's
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