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Satake, H.

Publications and source records attributed to Satake, H..

4 recordsLinked to original sources

Gamete release in Ciona robusta: roles of gonadotropin-releasing hormone and the photoreception system

Gamete release, an essential event for animals, is regulated by various factors including environmental stimuli, neural circuit, and endocrine molecules. In this study, we investigated the mechanisms regulating gamete release in the ascidian Ciona robusta, part of the sister group of vertebrates. Ciona is a hermaphrodite, releasing sperm first from orange-pigmented organ (OPO) at the end of the spermiduct, followed by eggs from the oviduct beneath the spermiduct knob-like structure. In this study, behavioral and morphological analyses revealed that this sequential release occurs because the knob-like structure compresses the oviduct opening at the onset of gamete release. Observations of transgenic Ciona expressing Kaede under the gonadotropin-releasing hormone 2 (Gnrh2) promoter showed that Gnrh2-expressing neurons and fibers accumulate in the epithelium around the spermiduct openings. In contrast, Gnrh1-expressing neurons are localized in the cerebral ganglion and project toward the ovary, suggesting distinct roles of GnRH1 and GnRH2 in reproductive regulation. RNA-seq and real-time PCR analyses revealed that Opsin2, Opsin3, beta-carotene-15,15-monooxygenase (Bco), and several ion channel genes are specifically expressed in the OPO, along with Gnrh2. In situ hybridization showed that these genes are localized in the innermost OPO layer, suggesting that the OPO functions as a photoreceptive organ. Although, Gnrh2 expression has been considered low in adult Ciona, our study revealed strong OPO-specific expression with photoreceptive genes. Collectively, these findings suggest that GnRH2 plays a central role in gamete release regulation, potentially in coordination with the photoreceptive system, while GnRH1 may regulate ovarian functions. These results indicate that C. robusta employs distinct GnRH systems in a tissue-specific manner to regulate reproduction.

evolutionary biology↗

Neural signaling contributes to heart formation and growth in the invertebrate chordate, Ciona robusta.

Neurons contribute to the complex interplay of signals that mediate heart development and homeostasis. Although a limited set of studies suggest that neuronal peptides impact vertebrate heart growth, the specific contributions of these peptides to cardiomyocyte progenitor differentiation or proliferation have not been elucidated. Here we show that the neuropeptide tachykinin along with canonical Wnt signaling regulate cardiomyocyte progenitor proliferation in the chordate model Ciona robusta. In C. robusta, the heart continues to grow throughout adulthood and classic histological studies indicate that a line of undifferentiated cells may serve as a reserve progenitor lineage. We found that this line of cardiomyocyte progenitors consists of distinct distal and midline populations. Distal progenitors divide asymmetrically to produce distal and midline daughters. Midline progenitors divide asymmetrically to produce myocardial precursors. Through single cell RNA sequencing (scRNA-seq) of adult C. robusta hearts, we delineated the cardiomyocyte progenitor expression profile. Based on this data we investigated the role of Wnt signaling in cardiomyocyte progenitor proliferation and found that canonical Wnt signaling is required to suppress excessive progenitor proliferation. The scRNA-seq data also identified a number of presumptive cardiac neural-like cells. Strikingly, we found that a subset of these neuronal cells appears to innervate the distal cardiomyocyte progenitors. Based on the expression of the tachykinin receptor in these neuronal cells, we blocked tachykinin signaling using pharmacological inhibitors and found that this drove reduced proliferation in the distal progenitor pool. Through targeted CRISPR-Cas9 knockdown we then demonstrated that both extrinsic tachykinin and intrinsic, cardiac tachykinin receptors are required for formation of the myocardial heart tube. This work provides valuable insights into how organisms may deploy neural signals to regulate organ growth in response to environmental or homeostatic inputs.

developmental biology↗

Stimulatory and inhibitory G-protein signaling relays drive cAMP accumulation for timely metamorphosis in the chordate Ciona

Larvae of the ascidian Ciona initiate metamorphosis tens of minutes after adhesion to a substratum via their adhesive organ. The gap between adhesion and metamorphosis initiation is suggested to ensure the rigidity of adhesion, allowing Ciona to maintain settlement after losing locomotive activity through metamorphosis. The mechanism producing the gap is unknown. Here, by combining gene functional analyses, pharmacological analyses, and live imaging, we propose that the gap represents the time required for sufficient cAMP accumulation to trigger metamorphosis. Not only the Gs pathway but also the Gi and Gq pathways are involved in the initiation of metamorphosis in the downstream signaling cascade of the neurotransmitter GABA, the known initiator of Ciona metamorphosis. The mutual crosstalk of stimulatory and inhibitory G-proteins functions as the accelerator and brake for cAMP production, ensuring the faithful initiation of metamorphosis at an appropriate time and in the right situation.

developmental biology↗

Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: insights from tissue-specific gene expression

Tissue/organ-specific genes (TSGs) are important not only for understanding organ development and function, but also for investigating the evolutionary lineages of organs in animals. Here, we investigate the TSGs of 9 adult tissues of an ascidian, Ciona intestinalis Type A (Ciona robusta), which lies in the important position of being the sister group of vertebrates. RNA-seq and qRT-PCR identified the Ciona TSGs in each tissue, and BLAST searches identified their homologs in zebrafish and mice. Tissue distributions of the vertebrate homologs were analyzed and clustered using public RNA-seq data for 12 zebrafish and 30 mouse tissues. Among the vertebrate homologs of the Ciona TSGs in the neural complex, 48% and 63% showed high expression in the zebrafish and mouse brain, respectively, suggesting that the central nervous system is evolutionarily conserved in chordates. In contrast, vertebrate homologs of Ciona TSGs in the ovary, pharynx, and intestine were not consistently highly expressed in the corresponding tissues of vertebrates, suggesting that these organs have evolved in Ciona-specific lineages. Intriguingly, more TSG homologs of the Ciona stomach were highly expressed in the vertebrate liver (17-29%) and intestine (22-33%) than in the mouse stomach (5%). Expression profiles for these gene suggest that the biological roles of the Ciona stomach are distinct from those of their vertebrate counterparts. Collectively, Ciona tissues were categorized into 3 groups: i) high similarity to the corresponding vertebrate tissues (neural complex and heart), ii) low similarity to the corresponding vertebrate tissues (ovary, pharynx, and intestine), and iii) low similarity to the corresponding vertebrate tissues, but high similarity to other vertebrate tissues (stomach, endostyle, and siphons). The present study provides transcriptomic catalogs of adult ascidian tissues and significant insights into the evolutionary lineages of the brain, heart, and digestive tract of chordates.

evolutionary biology↗