Expression of AmphiCoe, an amphioxus COE/EBF gene, in the developing central nervous system and epidermal sensory neurons

Abstract

The COE/EBF gene family marks a subset of prospective neurons in the vertebrate central and peripheral nervous system, including neurons deriving from some ectodermal placodes. Since placodes are often considered unique to vertebrates, we have characterised an amphioxus COE/EBF gene with the aim of using it as a marker to examine the timing and location of peripheral neuron differentiation. A single COE/EBF family member, AmphiCoe, was isolated from the amphioxus Branchiostoma floridae. AmphiCoe lies basal to the vertebrate COE/EBF genes in molecular phylogenetic analysis, suggesting that the duplications that formed the vertebrate COE/EBF family were specific to the vertebrate lineage. AmphiCoe is expressed in the central nervous system and in a small number of scattered ectodermal cells on the flanks of neurulae stage embryos. These cells become at least largely recessed beneath the ectoderm. Scanning electron microscopy was used to examine embryos in which the ectoderm had been partially peeled away. This revealed that these cells have neuronal morphology, and we infer that they are the precursors of epidermal primary sensory neurons. These characters lead us to suggest that differentiation of some ectodermal cells into sensory neurons with a tendency to sink beneath the embryonic surface represents a primitive feature that has become incorporated into placodes during vertebrate evolution.

Retinoic acid influences anteroposterior positioning of epidermal sensory neurons and their gene expression in a developing chordate (amphioxus)

“…The normal developmental transcription of AmphiCoe has been reported for amphioxus (17). This gene is homologous to vertebrate markers for neural cell precursors and differentiating neurons (25).…”

“…An evolutionary relationship between these epidermal sensory neurons of amphioxus and some vertebrate neurogenic placodes (especially the olfactory placode) has been tentatively suggested (14,15). In amphioxus, the epidermal sensory neurons are scattered individually along the anteroposterior axis on either side of the body (16), where they can first be detected morphologically at the late neurula stage (17). Initially there are Ϸ24 such cells per embryo, but their numbers steadily increase to several hundred during subsequent development (15).…”

“…Initially there are Ϸ24 such cells per embryo, but their numbers steadily increase to several hundred during subsequent development (15). Previous work on gene expression patterns in the developing epidermal ectoderm of amphioxus suggests an origin of these sensory neurons from general epidermal cells: starting at the neurula stage, scattered epidermal cells express AmphiHu, a homolog of a vertebrate pan-neuronal marker (18), and AmphiCoe, a homolog of vertebrate markers for neural precursors and neurons differentiating from them (17).…”

The single AmphiTrk receptor highlights increased complexity of neurotrophin signalling in vertebrates and suggests an early role in developing sensory neuroepidermal cells

“…Previous observations of adults and larvae have shown the presence of widespread ectodermal sensory cells in amphioxus (Bone and Best, 1978). More recently, scanning electron microscope (SEM) observations of mid-late neurula embryos show some of these cells to be morphologically differentiated by this stage (Mazet et al, 2004). Gene expression patterns of the pan-neuronal marker AmphiElav, in Development 132 (9) Research article tandem with other morphological evidence, suggest that the origin of these sensory neurons stems from general epidermal cells in the developing embryo (Satoh et al, 2001;BenitoGutiérrez et al, 2005).…”

Characterization of novel GPCR gene coding locus in amphioxus genome: Gene structure, expression, and phylogenetic analysis with implications for its involvement in chemoreception

“…Although the sensory cells of the peripheral nervous system of amphioxus have been studied extensively by microscopy (Frantz, 1923;Schulte and Riehl, 1977;Bone and Best, 1978;Baatrup, 1981Baatrup, , 1982Lacalli and Hou, 1999;, immunostaining (Yasui et al, 1998;Kaji et al, 2001), cell labeling and axon tracing by DiI (Holland and Yu, 2002), and gene expression Mazet et al, 2004), it is not known conclusively whether they are mechanosensory or chemosensory cells.…”