Fine-grained fate maps for the ophthalmic and maxillomandibular trigeminal placodes in the chick embryo

Abstract

Vertebrate cranial ectodermal placodes are transient, paired thickenings of embryonic head ectoderm that are crucial for the formation of the peripheral sensory nervous system: they give rise to the paired peripheral sense organs (olfactory organs, inner ears and anamniote lateral line system), as well as the eye lenses, and most cranial sensory neurons. Here, we present the first detailed spatiotemporal fate-maps in any vertebrate for the ophthalmic trigeminal (opV) and maxillomandibular trigeminal (mmV) placodes, which give rise to cutaneous sensory neurons in the ophthalmic and maxillomandibular lobes of the trigeminal ganglion. We used focal DiI and DiO labelling to produce eight detailed fate-maps of chick embryonic head ectoderm over approximately 24 h of development, from 0-16 somites. OpV and mmV placode precursors arise from a partially overlapping territory; indeed, some individual dyespots labelled both opV and mmV placode-derived cells. OpV and mmV placode precursors are initially scattered within a relatively large region of ectoderm adjacent to the neural folds, intermingled both with each other and with future epidermal cells, and with geniculate and otic placode precursors. Although the degree of segregation increases with time, there is no clear border between the opV and mmV placodes even at the 16-somite stage, long after neurogenesis has begun in the opV placode, and when neurogenesis is just beginning in the mmV placode. Finally, we find that occasional cells in the border region between the opV placode and mmV placode express both Pax3 (an opV placode specific marker) and Neurogenin1 (an mmV placode specific marker), suggesting that a few cells are responding to both opV and mmV placode-inducing signals. Overall, our results fill a large gap in our knowledge of the early stages of development of both the opV and mmV placodes, providing an essential framework for subsequent studies of the molecular control of their development.

Mechanisms of cranial placode assembly

“…In the fate mapping experiments described above, single labelled cells most often generated progeny in only one specific placode, even when the labelling occured before segregation (Bhattacharyya and Bronner, 2013;Dutta et al, 2005;Xu et al, 2008). This observation suggests that placodal progenitors are lineage-restricted before their spatial segregation (Bhattacharyya and Bronner, 2013;Dutta et al, 2005;Toro and Varga, 2007), although this needs to be more directly proven.…”

“…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).…”

“…The delamination process of trigeminal and epibranchial placodes was initially observed on sections of fixed tissues in mammals and in chick embryos (for example, see Blentic et al, 2011;Graham et al, 2007;Knabe et al, 2009;McCabe et al, 2009;Shiau et al, 2008;Xu et al, 2008), and by DiI labelling of the surface ectoderm in chick (Stark et al, 1997;Begbie, 2001a;McCabe et al, 2009). However, delamination of trigeminal or epibranchial cells from the ectoderm has to our knowledge not yet been directly observed in zebrafish or amphibian embryos, and its timing and modalities remain unclear in these species.…”

Essential role for PDGF signaling in ophthalmic trigeminal placode induction

“…lens and otic) that are morphologically distinct from neighboring ectoderm, trigeminal placode cells cannot be distinguished from surrounding tissue. Cell marking techniques suggest that the ectoderm overlying the presumptive midbrain and rostral hindbrain is fated to contribute to the trigeminal ganglion (Webb and Noden, 1983;Xu et al, 2008). Furthermore, the transcription factor Pax3 and the tetraspanin CD151 serve as molecular markers of the ophthalmic trigeminal placode (Stark et al, 1997;Baker et al, 1999;McCabe et al, 2004).…”