Adenohypophysis placodal precursors exhibit distinctive features within the rostral preplacodal ectoderm

Abstract

Placodes are discrete thickenings of the vertebrate cranial ectoderm that generate morpho-functionally distinct structures, such as the adenohypophysis, olfactory epithelium and lens. All placodes arise from a horseshoe-shaped preplacodal ectoderm in which the precursors of individual placodes are intermingled. However, fate-map studies indicated that cells positioned at the preplacodal midline give rise to only the adenohypophyseal placode, suggesting a unique organization of these precursors within the preplacode. To test this possibility, we combined embryological and molecular approaches in chick embryos to show that, at gastrula stage, adenohypophyseal precursors are clustered in the median preplacodal ectoderm, largely segregated from those of the adjacent olfactory placode. Median precursors are elongated, densely packed and, at neurula stage, express a molecular signature that distinguishes them from the remaining preplacodal cells. Olfactory placode precursors and midline neural cells can replace ablated adenohypophyseal precursors up to head-fold stage, although with a more plastic organization. We thus propose that adenohypophyseal placode precursors are unique within the preplacodal ectoderm possibly because they originate the only single placode and the only one with an endocrine character.

Neural plate progenitors give rise to both anterior and posterior pituitary cells

“…The pituitary is an evolutionarily conserved neuroendocrine organ of significant physiological importance. It has been well accepted its main tissue components, the AH and the NH, originate from the embryonic oral ectoderm and the neural ectoderm, respectively (De Beer, 1924; Herring, 1908; Sanchez-Arrones et al, 2017). Here, while dissecting the molecular attributes of zebrafish pituitary at a single cell level, we revealed that in contrast to the prevailing dogma, neural plate progenitors contribute to both adenohypophyseal and neurohypophyseal cell types.…”

“…It is noted that although the pre-placodal ectodermal origin of the AH cells is well established (Couly and Le Douarin, 1988; Dutta et al, 2005; Kouki et al, 2001; Sanchez-Arrones et al, 2017), two studies using radiolabeling in Xenopus or analyzing quail grafted-chick chimeras have suggested that portions of anterior neural ridge (ANR), namely the most anterior neural tissue that meets the non-neural ectoderm, gives rise to at least a part of the adenohypophyseal cells (Couly and Le Douarin, 1985; Eagleson et al, 1986). However, the methods used in these studies lacked single cell resolution.…”

Dissecting the neural divide: a continuous neurectoderm gives rise to the olfactory placode and bulb

“…Sensory modalities did not all arise at the same time, thus supporting a potentially non-uniform development and function of sensory systems in modern vertebrates where there are substantial differences between placodes in terms of early development, organogenesis and integration in the nervous system. For example, recent studies examining adenohypopyseal placode development have shown an early cellular and molecular heterogeneity where the cellular morphology and gene expression patterns are distinct from that of the flanking "pre-placode" domain, (Sanchez-Arrones et al, 2017).…”

Specification of sensory placode progenitors: signals and transcription factor networks

“…(Couly and Le Douarin, 1985, Couly and Le Douarin, 1987, D'Amico-Martel and Noden, 1983, Noden, 1992, focusing on stages just before or after placodes become morphologically distinct. More recent studies investigating the origin of placodes showed that a continuous and unique territory of sensory progenitors can first be identified at head process stages (Bhattacharyya et al, 2004, Sanchez-Arrones et al, 2017, Streit, 2002, Xu et al, 2008: labelling experiments reveal a continuous band of ectoderm surrounding the anterior neural plate that contains precursors for all sensory placodes and has therefore been termed the pre-placodal region (PPR). An equivalent territory has also been identified by fate mapping experiments in Xenopus and fish (Bhat and Riley, 2011, Dutta et al, 2005, Kozlowski et al, 1997, Pieper et al, 2011.…”