Induction and specification of cranial placodes

Abstract

Cranial placodes are specialized regions of the ectoderm, which give rise to various sensory ganglia and contribute to the pituitary gland and sensory organs of the vertebrate head. They include the adenohypophyseal, olfactory, lens, trigeminal, and profundal placodes, a series of epibranchial placodes, an otic placode, and a series of lateral line placodes. After a long period of neglect, recent years have seen a resurgence of interest in placode induction and specification. There is increasing evidence that all placodes despite their different developmental fates originate from a common panplacodal primordium around the neural plate. This common primordium is defined by the expression of transcription factors of the Six1/2, Six4/5, and Eya families, which later continue to be expressed in all placodes and appear to promote generic placodal properties such as proliferation, the capacity for morphogenetic movements, and neuronal differentiation. A large number of other transcription factors are expressed in subdomains of the panplacodal primordium and appear to contribute to the specification of particular subsets of placodes. This review first provides a brief overview of different cranial placodes and then synthesizes evidence for the common origin of all placodes from a panplacodal primordium. The role of various transcription factors for the development of the different placodes is addressed next, and it is discussed how individual placodes may be specified and compartmentalized within the panplacodal primordium. Finally, tissues and signals involved in placode induction are summarized with a special focus on induction of the panplacodal primordium itself (generic placode induction) and its relation to neural induction and neural crest induction. Integrating current data, new models of generic placode induction and of combinatorial placode specification are presented.

Origin and Early Development of the Posterior Lateral Line System of Zebrafish

“…Alternatively, it may be that the order between the acquisition of pan-placodal properties, and of modality-specific properties, is unimportant and that various placodes acquire their identity before or after panplacodal genes are expressed. This hypothesis may account for the difference in phenocritical periods for the inner ear and PLL system documented here, and for the evidence that the induction of PLL and otic placodes are separate (for review, see Baker and Bronner-Fraser, 2001), in contrast to the increasing evidence that the otic and epibranchial placodes arise from a larger group of precursor cells that, presumably, also forms the PLL system (Schlosser, 2006;Sun et al, 2007;Freter et al, 2008).…”

“…If several of these steps act in parallel rather than hierarchically, their temporal order would be irrelevant. In this view, pan-placodal genes would provide territories that have acquired distinct identities with a set of common attributes, such as delamination, epithelial-mesenchymal transition, or neurogenesis (Schlosser, 2006). The seemingly obvious idea "generic first, specific later" may therefore be misleading (for review, see Brunet and Ghysen, 1999).…”

“…Molecular markers such as eya1 and six1 expression reveal the existence of a horseshoe-shaped region surrounding the anterior neural plate around the tailbud stage (10 hpf). This region is supposed to define a preplacodal domain that is later subdivided into distinct placodes (for review, see Baker and Bronner-Fraser, 2001;Schlosser, 2006). The expression of both eya1 and six1 is later confined to some placodes, including lateral line placodes (Sahly et al, 1999;Bessarab et al, 2004;Schlosser, 2006).…”

“…It is currently believed that the PLL and inner ear are derived from a common posterior placode [together with epibranchial ganglia (for review, see Schlosser, 2006;Baker et al, 2008)]. To decide whether the primary and secondary PLL placodes are initially established as a single group of PLL precursor cells, or as two independent entities, we tried to interfere with the formation of the system.…”

Analyzing Somatosensory Axon Projections with the Sensory Neuron-SpecificAdvillinGene

“…These neurons have their cell bodies located in a series of ganglia: the dorsal root ganglia (DRG) for trunk sensory neurons, the trigeminal ganglia (TG), or the trigeminal mesencephalic nuclei (Me5) for face somatosensory neurons. All peripheral sensory neurons are derived either from neural crest cells (precursors for majority of the neurons) or from cells in the neurogenic placodes (origin for many of the cranioganglia neurons) (for review, see Streit, 2004;Schlosser, 2006). Somatosensory neurons possess two major axonal branches originated from one unipolar axon growing out of the cell body: a peripheral branch that innervates peripheral targets such as hair, skin, internal organs, and muscles and a central axon that projects collaterals into the spinal cord or the brainstem and forms topographic representations of the body (Willis and Coggeshall, 1988;Rowe and Iwamura, 2001).…”