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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    • "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.
    Developmental Biology 05/2014; 389(1). DOI:10.1016/j.ydbio.2014.01.021 · 3.55 Impact Factor
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    • "Rather the cells appeared to move without changing their relative positions within the PPR and with adjacent ectodermal territories, suggesting that individualization of placodes from the preplacodal ectoderm does not involve large-scale cell sorting in Xenopus (Pieper et al., 2011). Another study performed at a later developmental stage recently showed that cells of the epibranchial placode move actively to segregate into distinct subpopulations. "
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    ABSTRACT: Specialized sensory organs in the vertebrate head originate from thickenings in the embryonic ectoderm called cranial sensory placodes. These placodes, as well as the neural crest, arise from a zone of ectoderm that borders the neural plate. This zone separates into a precursor field for the neural crest that lies adjacent to the neural plate, and a precursor field for the placodes, called the pre-placodal region (PPR), that lies lateral to the neural crest. The neural crest domain and the PPR are established in response to signaling events mediated by BMPs, FGFs and Wnts, which differentially activate transcription factors in these territories. In the PPR, members of the Six and Eya families, act in part to repress neural crest specific transcription factors, thus solidifying a placode developmental program. Subsequently, in response to environmental cues the PPR is further subdivided into placodal territories with distinct characteristics, each expressing a specific repertoire of transcription factors that provides the necessary information for their progression to mature sensory organs. In this review we summarize recent advances in the characterization of the signaling molecules and transcriptional effectors that regulate PPR specification and its subdivision into placodal domains with distinct identities.
    Developmental Biology 05/2014; 389(1). DOI:10.1016/j.ydbio.2014.02.011 · 3.55 Impact Factor
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    • "During the course of embryonic development , the regions giving rise to these organs are first blurred ( meaning that a single cell can con - tribute to several organs ) , but the respective fates gradually become spatially restricted ( Whitlock & Westerfield , 2000 ; Pieper et al . 2011 ) . Given that the similar induction and specification mecha - nisms of the pan - placodal region have been identified in different vertebrate species ( Xenopus , zebrafish , chick and mouse ) , the pan - placodal region almost certainly seems to represent a conserved spatiotemporal domain of vertebrate embryonic period ( Schlosser , 20"
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    ABSTRACT: The vertebrate oral region represents a key interface between outer and inner environments, and its structural and functional design is among the limiting factors for survival of its owners. Both formation of the respective oral opening (primary mouth) and establishment of the food-processing apparatus (secondary mouth) require interplay between several embryonic tissues and complex embryonic rearrangements. Although many aspects of the secondary mouth formation, including development of the jaws, teeth or taste buds, are known in considerable detail, general knowledge about primary mouth formation is regrettably low. In this paper, primary mouth formation is reviewed from a comparative point of view in order to reveal its underestimated morphogenetic diversity among, and also within, particular vertebrate clades. In general, three main developmental modes were identified. The most common is characterized by primary mouth formation via a deeply invaginated ectodermal stomodeum and subsequent rupture of the bilaminar oral membrane. However, in salamander, lungfish and also in some frog species, the mouth develops alternatively via stomodeal collar formation contributed both by the ecto- and endoderm. In ray-finned fishes, on the other hand, the mouth forms via an ectoderm wedge and later horizontal detachment of the initially compressed oral epithelia with probably a mixed germ-layer derivation. A very intriguing situation can be seen in agnathan fishes: whereas lampreys develop their primary mouth in a manner similar to the most common gnathostome pattern, hagfishes seem to undergo a unique oropharyngeal morphogenesis when compared with other vertebrates. In discussing the early formative embryonic correlates of primary mouth formation likely to be responsible for evolutionary-developmental modifications of this area, we stress an essential role of four factors: first, positioning and amount of yolk tissue; closely related to, second, endoderm formation during gastrulation, which initiates the process and constrains possible evolutionary changes within this area; third, incipient structure of the stomodeal primordium at the anterior neural plate border, where the ectoderm component of the prospective primary mouth is formed; and fourth, the prime role of Pitx genes for establishment and later morphogenesis of oral region both in vertebrates and non-vertebrate chordates.
    Journal of Anatomy 07/2012; 222(1). DOI:10.1111/j.1469-7580.2012.01540.x · 2.10 Impact Factor
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