Origin and segregation of cranial placodes in Xenopus laevis

Brain Research Institute, University of Bremen, FB2, PO Box 330440, 28334 Bremen, Germany.
Developmental Biology (Impact Factor: 3.55). 12/2011; 360(2):257-75. DOI: 10.1016/j.ydbio.2011.09.024
Source: PubMed


Cranial placodes are local thickenings of the vertebrate head ectoderm that contribute to the paired sense organs (olfactory epithelium, lens, inner ear, lateral line), cranial ganglia and the adenohypophysis. Here we use tissue grafting and dye injections to generated fate maps of the dorsal cranial part of the non-neural ectoderm for Xenopus embryos between neural plate and early tailbud stages. We show that all placodes arise from a crescent-shaped area located around the anterior neural plate, the pre-placodal ectoderm. In agreement with proposed roles of Six1 and Pax genes in the specification of a panplacodal primordium and different placodal areas, respectively, we show that Six1 is expressed uniformly throughout most of the pre-placodal ectoderm, while Pax6, Pax3, Pax8 and Pax2 each are confined to specific subregions encompassing the precursors of different subsets of placodes. However, the precursors of the vagal epibranchial and posterior lateral line placodes, which arise from the posteriormost pre-placodal ectoderm, upregulate Six1 and Pax8/Pax2 only at tailbud stages. Whereas our fate map suggests that regions of origin for different placodes overlap extensively with each other and with other ectodermal fates at neural plate stages, analysis of co-labeled placodes reveals that the actual degree of overlap is much smaller. Time lapse imaging of the pre-placodal ectoderm at single cell resolution demonstrates that no directed, large-scale cell rearrangements occur, when the pre-placodal region segregates into distinct placodes at subsequent stages. Our results indicate that individuation of placodes from the pre-placodal ectoderm does not involve large-scale cell sorting in Xenopus.

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Available from: Gearld Wayne Eagleson, Feb 02, 2015
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    • "The validity of the marker sets was confirmed by considering genes whose expression has been shown previously to be restricted to specific cranial sensory ganglia. Thus trigeminal ophthalmic expressed PAX3[10,28,29]; trigeminal maxillomandibular/ophthalmic ganglia expressed DRG11303132; and nodose/petrosal ganglia expressed PHOX2B[11,21,333435. Our panel of markers included 7 genes expressed in the nodose ganglion but not in the petrosal ganglion. These included the HOX genes HOXB4, −D4, −B5, and -B6 (Fig. 4A) reflecting the well-known distribution of HOX gene expression along the rostro-caudal axis. "
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    ABSTRACT: Background The cranial sensory ganglia represent populations of neurons with distinct functions, or sensory modalities. The production of individual ganglia from distinct neurogenic placodes with different developmental pathways provides a powerful model to investigate the acquisition of specific sensory modalities. To date there is a limited range of gene markers available to examine the molecular pathways underlying this process. Results Transcriptional profiles were generated for populations of differentiated neurons purified from distinct cranial sensory ganglia using microdissection in embryonic chicken followed by FAC-sorting and RNAseq. Whole transcriptome analysis confirmed the division into somato- versus viscerosensory neurons, with additional evidence for subdivision of the somatic class into general and special somatosensory neurons. Cross-comparison of distinct ganglia transcriptomes identified a total of 134 markers, 113 of which are novel, which can be used to distinguish trigeminal, vestibulo-acoustic and epibranchial neuronal populations. In situ hybridisation analysis provided validation for 20/26 tested markers, and showed related expression in the target region of the hindbrain in many cases. Conclusions One hundred thirty-four high-confidence markers have been identified for placode-derived cranial sensory ganglia which can now be used to address the acquisition of specific cranial sensory modalities. Electronic supplementary material The online version of this article (doi:10.1186/s13064-016-0057-y) contains supplementary material, which is available to authorized users.
    Full-text · Article · Dec 2016 · Neural Development
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    • "These works used either injections of the fluorescent lipophilic vital dyes DiI/DiO or retrovirus-mediated lineage analysis (Abelló et al., 2007; Bell et al., 2008; Brigande et al., 2000a; Kil and Collazo, 2001; Kozlowski et al., 1997; Lang and Fekete, 2001; Li et al., 1978; Pieper et al., 2011; Satoh and Fekete, 2005; Stevenson et al., 2012; Streit, 2002; Xu et al., 2008). Some of the studies were performed before the otic and trigeminal placodes were constituted as two separate identities (Kozlowski et al., 1997; Pieper et al., 2011; Streit, 2002), and a single study of the frog inner ear was carried out exactly at the otic placode stage (Kil and Collazo, 2001). Other studies addressed otic cup stages (Abelló et al., 2007; Bell et al., 2008; Brigande et al., 2000a) or otocyst stages (Kil and Collazo, 2001; Li et al., 1978), i.e. examined otic primordia that had already initiated important morphogenetic changes. "
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    ABSTRACT: The inner ear is an intricate three-dimensional sensory organ that arises from a flat, thickened portion of the ectoderm termed the otic placode. There is evidence that the ontogenetic steps involved in the progressive specification of the highly specialized inner ear of vertebrates involve the concerted actions of diverse patterning signals that originate from nearby tissues, providing positional identity and instructive context. The topology of the prospective inner ear portions at placode stages when such patterning begins has remained largely unknown. The chick-quail model was used to perform a comprehensive fate mapping study of the chick otic placode, shedding light on the precise topological position of each presumptive inner ear component relative to the dorsoventral and anteroposterior axes of the otic placode and, implicitly, to the possible sources of inducing signals. The findings reveal the existence of three dorsoventrally arranged anteroposterior domains from which the endolymphatic system, the maculae and basilar papilla, and the cristae develop. This study provides new bases for the interpretation of earlier and future descriptive and experimental studies that aim to understand the molecular genetic mechanisms involved in otic placode patterning.
    Full-text · Article · May 2014 · Development
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    • "Indeed, in zebrafish, lineage tracing reveals that Pax2 þ cells contribute to both the otic and facial (geniculate) placode (McCarroll et al., 2012). In chick, cells from the Pax2 and Sox3 positive regions converge to the placodes as the gene expression domains segregate (Ishii et al., 2001; Streit, 2002), while lineage tracing in Xenopus reveals an overlap between otic and epibranchial precursors (Pieper et al., 2011). As the placode territory splits, neural crest cells from the hyoid and branchial streams (2nd and 3rd streams) migrate around the otic placode and come to reside adjacent to both the facial and the combined glossopharyngeal/vagal (petrosal/nodose) placodes (Culbertson et al., 2011). "
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    ABSTRACT: In the vertebrate head, the peripheral components of the sensory nervous system are derived from two embryonic cell populations, the neural crest and cranial sensory placodes. Both arise in close proximity to each other at the border of the neural plate: neural crest precursors abut the future central nervous system, while placodes originate in a common pre-placodal region slightly more lateral. During head morphogenesis, complex events organise these precursors into functional sensory structures, raising the question of how their development is coordinated. Here we review the evidence that neural crest and placode cells remain in close proximity throughout their development and interact repeatedly in a reciprocal manner. We also review recent controversies about the relative contribution of the neural crest and placodes to the otic and olfactory systems. We propose that a sequence of mutual interactions between the neural crest and placodes drives the coordinated morphogenesis that generates functional sensory systems within the head.
    Full-text · Article · May 2014 · Developmental Biology
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