Abstract
ABSTRACTThe embryonic development of the pineal organ, a neuroendocrine gland on top of the diencephalon, remains enigmatic. Classic fate-mapping studies suggested that pineal progenitors originate from the lateral border of the anterior neural plate. We show here, using gene expression and fate mapping/lineage tracing in zebrafish, that pineal progenitors originate, at least in part, from the non-neural ectoderm. Gene expression in chick indicates that this non-neural origin of pineal progenitors is conserved in amniotes. Genetic repression of placodal, but not neural crest, cell fate results in pineal hypoplasia in zebrafish, while mis-expression of transcription factors known to specify placodal identity during gastrulation promotes the formation of ectopic pineal progenitors. We also demonstrate that fibroblast growth factors (FGFs) position the pineal progenitor domain within the non-neural border by repressing pineal fate and that the Otx transcription factors promote pinealogenesis by inhibiting this FGF activity. The non-neural origin of the pineal organ reveals an underlying similarity in the formation of the pineal and pituitary glands, and suggests that all CNS neuroendocrine organs may require a non-neural contribution to form neurosecretory cells.
Highlights
The pineal organ, one of the circumventricular organs, is an endocrine gland located above the diencephalon in the brain of most vertebrates
The most anterior part of the irx1b-positive preplacodal region (PPR) that is known to give rise to the trigeminal placode expresses neurogenin 1, which encodes a basic helix-loop-helix transcription factor involved in neurogenesis (Fig. 1B,E-H). irx1b is expressed in the posterior neural plate, but the prospective neural crest that lies between the posterior neural plate and PPR, and is marked by expression of foxd3, is irx1b negative (Fig. 1F,H)
When we analysed the expression of the bona fide pineal progenitor marker flh/noto in relation to these different domains, we found that its territory reaches further laterally than the expression of irx1b in the neural plate (Fig. 1C,D), suggesting that it might extend into the neural crest and/or PPR domain
Summary
The pineal organ ( known as pineal gland or epiphysis cerebri), one of the circumventricular organs, is an endocrine gland located above the diencephalon in the brain of most vertebrates. The human pineal organ is about half a centimetre in length and can be found in the superior cistern, wedged in between the cerebral hemispheres. The pineal organ contains photoreceptors that molecularly and structurally resemble the photoreceptors of the retina. This has led to the suggestion that the pineal organ represents a phylogenetically ancient photosensitive organ that may have lost its Department for Developmental Neurobiology, Guy’s Hospital Campus, King’s College London, London SE1 1UL, UK. *Present address: Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK.
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