Expression of neuropeptide- and hormone-encoding genes in the Ciona intestinalis larval brain

Abstract

Despite containing only approximately 330 cells, the central nervous system (CNS) of Ciona intestinalis larvae has an architecture that is similar to the vertebrate CNS. Although only vertebrates have a distinct hypothalamus-the source of numerous neurohormone peptides that play pivotal roles in the development, function, and maintenance of various neuronal and endocrine systems, it is suggested that the Ciona brain contains a region that corresponds to the vertebrate hypothalamus. To identify genes expressed in the brain, we isolated brain vesicles using transgenic embryos carrying Ci-β-tubulin(promoter)::Kaede, which resulted in robust Kaede expression in the larval CNS. The associated transcriptome was investigated using microarray analysis. We identified 565 genes that were preferentially expressed in the larval brain. Among these genes, 11 encoded neurohormone peptides including such hypothalamic peptides as gonadotropin-releasing hormone and oxytocin/vasopressin. Six of the identified peptide genes had not been previously described. We also found that genes encoding receptors for some of the peptides were expressed in the brain. Interestingly, whole-mount in situ hybridization showed that most of the peptide genes were expressed in the ventral brain. This catalog of the genes expressed in the larval brain should help elucidate the evolution, development, and functioning of the chordate brain.

Three-dimensional anatomy of the Ciona intestinalis tailbud embryo at single-cell resolution

“…These cells might correspond to tail bipolar neurons, because the location and soma shape of the bipolar cells is similar to the reported for bipolar neuron cells with g-aminobutyric acid (GABA)-like immunoreactivity in Ciona (Brown et al, 2005). In addition, the location of expression of Ci-GnRHR4 and a newly-identified candidate peptide gene CLSTR16011 (Hamada et al, 2011), were in part similar in this region. Therefore, the cell lineage of this unidentified cells might be derived from b/b n 7.13 blastomeres of tail bipolar neurons.…”

“…Because of its similar location, it might be same tissue as the one we found. Interestingly, Ci-TK (tachykinin gene) was expressed in the anterior ventral brain at the tailbud stage, an expression domain that expanded around the pigmented cells in the larval brain (Hamada et al, 2011). Thus, the Ci-TK-positive cells might correspond to the unidentified cells at the lateral side of the ventral SV in this study.…”

Vertebrate Cranial Placodes as Evolutionary Innovations—The Ancestor's Tale

“…Expression of these various hormones in tunicates is concentrated in the CNS (Hamada et al, 2011), and GPA2 and GPB5, which are not well characterized in tunicates, are expressed in the CNS of both arthropods and amphioxus (Dos Santos, Mazan, Venkatesh, Cohen-Tannoudji, & Querat, 2011;Sellami, Agricola, & Veenstra, 2011;Tando & Kubokawa, 2009). This suggests a possible origin of the adenohypophyseal neurosecretory cells from the CNS.…”

Localization of Neuropeptide Gene Expression in Larvae of an Echinoderm, the Starfish Asterias rubens

“…The expression patterns of genes encoding gonadotropin-releasing hormone (GnRH)-type, oxytocin/vasopressin-type, tachykinin-type, and galanin-type peptides have been mapped and they suggest that these neuropeptides play roles in regulation of osmotic pressure, sensing of environmental cues, larval movement, and initiation of metamorphosis (Hamada et al, 2011). More recently, the genome sequences of hemichordate species have been determined (Simakov et al, 2015), but as yet there has been little investigation of neuropeptide systems in these animals.…”