Origin and segregation of cranial placodes in Xenopus laevis

Abstract

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.

Sp8 regulates inner ear development

“…Earlier studies of lineage analysis and spatiotemporal expression of transcription factors during inner ear development led to construction of an inner ear fate map in Xenopus and this fate map allows us to interpret gene expression patterns within the context of the anatomy (8,9). In recent years, genetic and genomic approaches have been developed in Xenopus tropicalis (10)(11)(12)(13).…”

Mechanisms of cranial placode assembly

“…These studies showed that sensory placodes arise from a crescent-shaped ectodermal territory surrounding the anterior neural plate at late gastrulation/ early neurulation stages. This contiguous region coincides with the expression domain of transcription factors such as Eya1, Six1/2 and Six4/5, which are crucial for placode formation and are thought to establish a placodal bias in this domain (Lleras-Forero and Streit, 2012;Pieper et al, 2011;Schlosser, 2010). These observations, together with unique properties shared by cells within this territory Martin and Grooves, 2006), argue that it represents the common domain of origin for all placodes, the so-called pan-placodal or pre-placodal region (PPR) Schlosser, 2010;Streit, 2008).…”

“…Although information is still incomplete in some species about subsets of placodes, a common feature of these fate mapping studies is the initial overlap between the domains of origin of the different placodes (the extent of this overlap has been recently discussed and challenged, for details see Pieper et al, 2011;Schlosser, 2010), which progressively decreases as development proceeds. That is, the precursors of a given placode appear scattered within the PPR domain and partially intermingled with the precursors of adjacent placodes as well as with other ectodermal cells such as epidermal, neural tube or neural crest cells (NCC), and undergo progressive segregation over time, becoming confined to a particular region ( Fig.…”

“…That is, the precursors of a given placode appear scattered within the PPR domain and partially intermingled with the precursors of adjacent placodes as well as with other ectodermal cells such as epidermal, neural tube or neural crest cells (NCC), and undergo progressive segregation over time, becoming confined to a particular region ( Fig. 1) (Kozlowski et al, 1997;Bhattacharyya and Bronner, 2013;Dutta et al, 2005;Pieper et al, 2011;Streit, 2002;Whitlock and Westerfield, 2000;Xu et al, 2008). This initial segregation leads to the formation of distinct placodal compartments that are still apposed to each other at early somitogenesis stages (Fig.…”

“…The formation of segregated placode primordia correlates in time with upregulation of transcription factors specifically expressed in individual or groups of placodes Pieper et al, 2011;Schlosser, 2010;Streit, 2008). Pax2 and Pax8, expressed in the otic and epibranchial placode progenitors (and in lateral line placodes in fish and amphibians), show saltand-pepper expression in chick (Groves and Bronner-Fraser, 2000;Streit, 2002), Xenopus (Pieper et al, 2011;Schlosser and Ahrens, 2004), zebrafish (Bhat et al, 2013;Bhat and Riley, 2011;Hans and Westerfield, 2007;McCarroll et al, 2012; Kozlowski et al, 1997;Bhattacharyya and Bronner, 2013;Breau et al, 2012;Dutta et al, 2005;Harden et al, 2012;Knaut et al, 2005;Kwan et al, 2011;Pieper et al, 2011;Streit, 2002;Whitlock and Westerfield, 2000;Xu et al, 2008) al., 2012) and mice (Ohyama and Groves, 2004). Pax6, a transcription factor expressed in the lens placode, exhibit mosaic expression in zebrafish (Dutta et al, 2005;Hans and Westerfield, 2007).…”