Ion fluxes through membrane ion channels play crucial roles both in neuronal signaling and the homeostatic control of body electrolytes. Despite our knowledge about the respective ion channels, just how diversification of ion channel genes underlies adaptation of animals to the physical environment remains unknown. Here we systematically survey up to 160 putative ion channel genes in the genome of Ciona intestinalis and compare them with corresponding gene sets from the genomes of the nematode Chaenorhabditis elegans, the fruit fly Drosophila melanogaster, and the more closely related genomes of vertebrates. Ciona has a set of so-called "prototype" genes for ion channels regulating neuronal excitability, or for neurotransmitter receptors, suggesting that genes responsible for neuronal signaling in mammals appear to have diversified mainly via gene duplications of the more restricted members of ancestral genomes before the ascidian/vertebrate divergence. Most genes responsible for modulation of neuronal excitability and pain sensation are absent from the ascidian genome, suggesting that these genes arose after the divergence of urochordates. In contrast, the divergent genes encoding connexins, transient receptor potential-related channels and chloride channels, channels involved rather in homeostatic control, indicate gene duplication events unique to the ascidian lineage. Because several invertebrate-unique channel genes exist in Ciona genome, the crown group of extant vertebrates not only acquired novel channel genes via gene/genome duplications but also discarded some ancient genes that have persisted in invertebrates. Such genome-wide information of ion channel genes in basal chordates enables us to begin correlating the innovation and remodeling of genes with the adaptation of more recent chordates to their physical environment.
During early ascidian development, which is a prototype of early vertebrate development, anterior neuroectoderm cells (a4.2) from the eight-cell embryo are destined to become anterior neural structures including the brain vesicle, while presumptive notochordal neural cells (A4.1) become larval posterior neural structures including motoneurons. Whereas, an anterior quadrant cell (A3) of the four-cell embryo, from which both anterior neuroectoderm (a4.2) and notochordal neural cells (A4.1) are derived, has both fates. Cleavage-arrested cell triplets were prepared from the anterior quadrant cell and a pair of anterior neuroectoderm cells (A3-aa triplet) or a pair of presumptive notochordal neural cells (A3-AA triplet), and cultured in contact. Differentiation of cells in the triplet was determined electrophysiologically by observing cell type-specific currents. In the A3-aa triplet, when two neuroectoderm cells and an anterior quadrant cell were prepared from the same batch of embryos, all three cells in the triplet developed into neuronal cells in 60 % of cases, but in 40 % of cases all of them differentiated into epidermal cells. However, when the batch of embryos from which neuroectoderm cells were prepared was fertilized 3 h later than that from which the anterior quadrant cell was prepared all three cells in the triplet consistently became neuronal cells. In contrast, when the batch of embryos from which neuroectoderm cells were prepared was fertilized 3 h earlier, all three cells became epidermal. In the A3-AA triplet no switching of differentiation occurred and all three cells in the triplet differentiated into neuronal cells, although the amplitude of inward current was often small. In neuralized A3-aa triplets the spikes in the anterior quadrant cell were characteristically small in amplitude and brief in duration, suggesting the presence of A-currents, which is a characteristic feature of posterior neuronal differentiation. In contrast, the spikes in the anterior neuroectoderm cells were large in amplitude and long in duration, chracteristic to the anterior neuronal type. The majority of single isolated anterior quadrant cells became non-excitable. However, the minority was apparently autonomously neuralized to become the posterior neuronal type. In neuralized A3-AA triplets, the majority of anterior quadrant cells was induced to become the anterior neuronal type. When isolated anterior quadrant cells were neuralized with subtilisin, a protease, they also predominantly became the anterior neuronal type. While, in medium containing a fibroblast growth factor posterior neuralization of isolated anterior quadrant cells was facilitated, but the anterior neuronal type, although minor, appeared anew. These observations indicate that the multiple fates of the anterior quadrant cell expressed in vivo were effectively reproduced in this experimental condition at the single cell level. Interactive differentiation in this triplet system recapitulates not only fundamental neural induction of ascidian neuroectoderm ce...
Background: In spite of the recent accumulation of genomic data, the evolutionary pathway in the individual genes of present-day living taxa is still elusive for most genes. Among ion channels, inward K + rectifier (IRK) channels are the fundamental and well-defined protein group. We analyzed the genomic structures of this group and compared them among a phylogenetically wide range with our sequenced Halocynthia roretzi, a tunicate, IRK genomic genes.
According to the evolutionary tree proposed by Garstang, the tunicate larva has a central role in directing the ancestral sessile animal derived from primitive echinoderms into the stem for vertebrates by evolution through neoteny. The close similarity of the tunicate larval body plan to those of vertebrates and the extraordinary simplicity indicated by an extremely small cell population make the ascidian embryo and larva an excellent model system for analysis of vertebrate embryonic development. Furthermore, isolated anterior animal blastomeres from the Halocynthia eight‐cell cleavage‐arrested embryo, which are known to include presumptive brain vesicle region, autonomously develop long‐lasting Ca‐dependent action potentials which are characteristic of epidermal differentiation. However, when blastometeres are cultured in contact with the anterior vegetal blastomere, which are known to include presumptive notochordal region, and raised in contacted two cell systems, the same anterior animal blastomeres now develop neuronal Na+ spikes characterized by expression of Na+ channels and triethylammonium sensitive delayed rectifier K+ channels. This unique two‐cell system enables us to examine roles of cell contact in various aspects of inductive differentiation at the cellular level. In this review, we focus on this simple cellular preparation and in particular, attempt to show how to make the preparation. © 1998 John Wiley & Sons, Inc. J Neurobiol 37: 3–22, 1998
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