Comparative analysis of transcriptomic profiles among ascidians, zebrafish, and mice: Insights from tissue-specific gene expression DOI Creative Commons
Shin Matsubara, Tomohiro Osugi, Akira Shiraishi

et al.

PLoS ONE, Journal Year: 2021, Volume and Issue: 16(9), P. e0254308 - e0254308

Published: Sept. 24, 2021

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

Language: Английский

A Nearly Complete Genome of Ciona intestinalis Type A (C. robusta) Reveals the Contribution of Inversion to Chromosomal Evolution in the Genus Ciona DOI Creative Commons
Yutaka Satou, Ryohei Nakamura,

Deli Yu

et al.

Genome Biology and Evolution, Journal Year: 2019, Volume and Issue: 11(11), P. 3144 - 3157

Published: Oct. 15, 2019

Abstract Since its initial publication in 2002, the genome of Ciona intestinalis type A (Ciona robusta), first sequence an invertebrate chordate, has provided a valuable resource for wide range biological studies, including developmental biology, evolutionary and neuroscience. The assembly was updated 2008, it included 68% information 14 pairs chromosomes. However, more contiguous is required analyses higher order genomic structure chromosomal evolution. Here, we provide new inbred line this animal, constructed with short long sequencing reads Hi-C data. In latest assembly, over 95% 123 Mb data Short predicted size 114–120 Mb; therefore, likely that current contains almost entire genome, although estimate smaller than previous estimates. Remapping onto revealed large inversion line. Moreover, comparison savignyi, different species same genus, many inversions between these two species, suggesting such have occurred frequently contributed to evolution species. Thus, present greatly improves essential genome-wide studies ascidians.

Language: Английский

Citations

104

Ovarian tachykinin signaling system induces the growth of secondary follicles during the gonadotropin-independent process DOI Creative Commons
Tsuyoshi Kawada, Masato Aoyama, Shin Matsubara

et al.

Journal of Biological Chemistry, Journal Year: 2025, Volume and Issue: unknown, P. 108375 - 108375

Published: March 1, 2025

Mammalian follicle growth development is mainly regulated by the hypothalamus-pituitary-gonadal (HPG) axis after puberty. Although pituitary hormones, gonadotropins, are involved in HPG signaling, they not responsible for of early-stage follicles, namely, primordial primary and secondary both sexually immature mature individuals. Unlike those gonadotropin-dependent growth, specific regulatory factors gonadotropin-independent have yet to be identified. Here, we identified tachykinins (TKs) as inducers growth. TKs play various roles neuropeptides or hormones a wide variety biological events central nervous system peripheral tissues, but direct effect on ovarian follicles has investigated. Follicle was suppressed 3-week-old knockout mice Tac1 gene encoding (substance P neurokinin A), which independent gonadotropins. their receptors specifically localized granulosa cells mouse follicles. Furthermore, upregulate prostaglandin (PG) synthase COX-2 via JAK1-STAT3 signaling cascade. We also demonstrated that PGE2 PGF2α major PGs ovary, enhanced interaction between / receptors, receptor (EP2) oocyte membrane (FP) membrane, cells, theca cells. Consequently, this study paves way exploring systems relevant dysfunctions, including pediatric endocrinological diseases.

Language: Английский

Citations

1

Repertoires of G protein-coupled receptors for Ciona -specific neuropeptides DOI Creative Commons
Akira Shiraishi,

Toshimi Okuda,

Natsuko Miyasaka

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2019, Volume and Issue: 116(16), P. 7847 - 7856

Published: April 1, 2019

Neuropeptides play pivotal roles in various biological events the nervous, neuroendocrine, and endocrine systems, are correlated with both physiological functions unique behavioral traits of animals. Elucidation functional interaction between neuropeptides receptors is a crucial step for verification their evolutionary processes. However, most novel peptides remain to be identified. Here, we show identification multiple G protein-coupled (GPCRs) species-specific vertebrate sister group, Ciona intestinalis Type A, by combining machine learning experimental validation. We developed an original peptide descriptor-incorporated support vector used it predict 22 neuropeptide-GPCR pairs. Of note, signaling assays predicted pairs identified 1 homologous 11 Ciona-specific 41% hit rate: respective GPCRs Ci-GALP, Ci-NTLP-2, Ci-LF-1, Ci-LF-2, Ci-LF-5, Ci-LF-6, Ci-LF-7, Ci-LF-8, Ci-YFV-1, Ci-YFV-3. Interestingly, molecular phylogenetic tree analysis revealed that these receptors, excluding Ci-GALP receptor, were evolutionarily unrelated any other known GPCRs, confirming constitute unprecedented neuropeptide receptor clusters. Altogether, results verified protochordate lineages pave way investigating endogenous closest relatives vertebrates processes neuropeptidergic systems throughout chordates. In addition, present study also indicates versatility machine-learning-assisted strategy peptide-receptor organisms.

Language: Английский

Citations

43

Reproductive roles of the vasopressin/oxytocin neuropeptide family in teleost fishes DOI Creative Commons
Jan A. Mennigen, Divya Ramachandran, Katherine Shaw

et al.

Frontiers in Endocrinology, Journal Year: 2022, Volume and Issue: 13

Published: Oct. 13, 2022

The vertebrate nonapeptide families arginine vasopressin (AVP) and oxytocin (OXT) are considered to have evolved from a single vasopressin-like peptide present in invertebrates termed vasotocin early evolution. Unprecedented genome sequence availability has more recently allowed new insight into the evolution of nonapeptides especially their receptor context whole duplications. In bony fish, homologues AVP (Avp) an OXT family (Oxt) originally isotocin been characterized. While reproductive roles both historically studied several vertebrates, teleost reproduction remain much less understood. Taking advantage novel resources associated technological advances such as genetic modifications fish models, we here critically review current state knowledge regarding systems reproduction. We further discuss sources plasticity conserved diverse phenotypes observed fishes. Given dual preoptic area (POA) synthesized Avp Oxt neuromodulators endocrine/paracrine factors, focus on known peptides behaviour regulation hypothalamic-pituitary-gonadal axis. Emphasis is placed identification gonadal system that plays critical steroidogenesis gamete maturation. conclude by highlighting key research gaps including call for translational studies linking mechanistic understanding regulated physiology aquaculture, conservation biology ecotoxicology.

Language: Английский

Citations

26

Comparative and Evolutionary Physiology of Vasopressin/ Oxytocin-Type Neuropeptide Signaling in Invertebrates DOI Creative Commons

Esther Odekunle,

Maurice R. Elphick

Frontiers in Endocrinology, Journal Year: 2020, Volume and Issue: 11

Published: April 17, 2020

The identification of structurally related hypothalamic hormones that regulate blood pressure and diuresis (vasopressin, VP; CYFQNCPRG-NH2) or lactation uterine contraction (oxytocin, OT; CYIQNCPLG-NH2) was a major advance in neuroendocrinology, recognised the award Nobel Prize for Chemistry 1955. Furthermore, discovery central actions VP OT as regulators reproductive social behaviour humans other mammals has broadened interest these neuropeptides beyond physiology into psychology. VP/OT-type their G-protein coupled receptors originated common ancestor Bilateria (Urbilateria), with invertebrates typically having single neuropeptide cognate receptor. Gene/genome duplications followed by gene loss gave rise to variety number different vertebrate lineages. Recent advances comparative transcriptomics/genomics have enabled an ever-growing diversity invertebrate taxa, providing new opportunities gain insights evolution function Bilateria. Here we review invertebrates, roles regulation reproduction, feeding water/salt homeostasis emerging themes. For example, highlight recent reports oocyte maturation sea-squirt Ciona intestinalis, extraoral starfish Asterias rubens energy status dessication resistance ants. Thus, are pleiotropic physiological processes, evolutionarily conserved can be traced back Urbilateria. To deeper understanding it may necessary not only determine peptides but also characterise transcriptomic/proteomic/metabolomic profiles cells expressing precursors and/or within framework anatomically functionally identified neuronal networks. investigation wider range species is now needed if how when this ancient signalling system recruited diverse behavioural processes branches animal phylogeny contrasting environmental contexts.

Language: Английский

Citations

38

Knock-out of vasotocin reduces reproductive success in female zebrafish, Danio rerio DOI Creative Commons
Divya Ramachandran,

Kusum Sharma,

Vishal Saxena

et al.

Frontiers in Endocrinology, Journal Year: 2023, Volume and Issue: 14

Published: Aug. 21, 2023

The vertebrate nonapeptide vasotocin/vasopressin is evolutionarily highly conserved and acts as neuromodulator endocrine/paracrine signaling molecule. Circumstantial mechanistic evidence from pharmacological manipulations of the vasotocin system in several teleost fishes suggest sex- species-specific reproductive roles vasotocin. While effects on physiology involve both courtship behaviors regulation hypothalamic-pituitary-gonadal (HPG) axes, comprehensive studies investigating behavioral physiological consequences genetic ablation a genetically tractable fish model, such zebrafish, are currently lacking. Here, we report generation homozygous CRISPR/Cas9-based gene knock-out zebrafish. Breeding pairs produce significantly fewer fertilized eggs per clutch compared to wildtype fish, an effect coincident with reduced female quivering behavior. Crossbreeding experiments reveal that this phenotype entirely female-dependent, vasotocin-deficient males reproduce normally when paired wild-type fish. Histological analyses ovaries revealed overall reduction oocytes differential distribution oocyte maturation stages, demonstrating linked release. Ovarian hormone quantification expression analysis mutant indicated synthesis Prostaglandin F2α, involved ovarian maturation, egg release behavior some cyprinids. However, acute injection did not rescue phenotype, suggesting contribution organizational Together, study provides further support for emerging reproduction important model species.

Language: Английский

Citations

11

Managing the Oocyte Meiotic Arrest—Lessons from Frogs and Jellyfish DOI Creative Commons
Catherine Jessus, Catriona Munro, Evelyn Houliston

et al.

Cells, Journal Year: 2020, Volume and Issue: 9(5), P. 1150 - 1150

Published: May 7, 2020

During oocyte development, meiosis arrests in prophase of the first division for a remarkably prolonged period firstly during growth, and then when awaiting appropriate hormonal signals egg release. This arrest is finally unlocked locally produced maturation initiation hormones (MIHs) trigger entry into M-phase. Here, we assess current knowledge successive cellular molecular mechanisms responsible keeping meiotic progression on hold. We focus two model organisms, amphibian Xenopus laevis, hydrozoan jellyfish Clytia hemisphaerica. Conserved govern initial programme prior to growth also, much later, onset mitotic divisions, via activation key kinase systems: Cdk1-Cyclin B/Gwl (MPF) M-phase Mos-MAPkinase orchestrate polar body formation cytostatic (CSF) arrest. In contrast, maintenance state fully-grown assured by highly specific mechanisms, reflecting enormous variation between species MIHs, MIH receptors their immediate downstream signalling response. Convergence multiple pathway components promote MPF some oocytes, including Xenopus, likely heritage complex evolutionary history spawning regulation, but also helps ensure robust reliable mechanism gamete production.

Language: Английский

Citations

31

Evolution of Neuropeptide Signaling: From a Single Cell to Mammals DOI
Quirin Krabichler, Valery Grinevich

Masterclass in neuroendocrinology, Journal Year: 2025, Volume and Issue: unknown, P. 3 - 43

Published: Jan. 1, 2025

Language: Английский

Citations

0

A Testis-Specific Long Noncoding RNA, Start, Is a Regulator of Steroidogenesis in Mouse Leydig Cells DOI Creative Commons
Kai Otsuka, Shin Matsubara, Akira Shiraishi

et al.

Frontiers in Endocrinology, Journal Year: 2021, Volume and Issue: 12

Published: April 1, 2021

The testis expresses many long noncoding RNAs (lncRNAs), but their functions and overview of lncRNA variety are not well understood. mouse Prss/Tessp locus contains six serine protease genes two lncRNAs that have been suggested to play important roles in spermatogenesis. Here, we found a novel testis-specific lncRNA, Start ( Steroidogenesis activating ), this locus. is 1822 nucleotides length was be localized mostly the cytosol germ cells Leydig cells, although nuclear localization also observed. -knockout (KO) mice generated by CRISPR/Cas9 system were fertile showed no morphological abnormality adults. However, adult -KO testes, RNA-seq qRT-PCR analyses revealed an increase expression steroidogenic such as Star Hsd3b1 , while ELISA analysis testosterone levels serum significantly low. Interestingly, at 8 days postpartum, both gene level decreased mice. Since overexpression Leydig-derived cell lines resulted elevation including likely involved upregulation. testes might caused secondary effect via androgen receptor autocrine pathway or hypothalamus-pituitary-gonadal axis. Additionally, observed reduced number postpartum. Collectively, our results strongly suggest regulator steroidogenesis cells. current study provides insight into overall picture function lncRNAs.

Language: Английский

Citations

21

Kobayashi Award 2021: Neuropeptides, receptors, and follicle development in the ascidian, Ciona intestinalis Type A: New clues to the evolution of chordate neuropeptidergic systems from biological niches DOI Creative Commons
Honoo Satake

General and Comparative Endocrinology, Journal Year: 2023, Volume and Issue: 337, P. 114262 - 114262

Published: March 15, 2023

Ciona intestinalis Type A (Ciona robusta) is a cosmopolitan species belonging to the phylum Urochordata, invertebrate chordates that are phylogenetically most closely related vertebrates. Therefore, this of interest for investigation evolution and comparative physiology endocrine, neuroendocrine, nervous systems in chordates. Our group has identified>30 neuropeptides (80% all identified ascidian neuropeptides) primarily using peptidomic approaches combined with reference genome sequences. These classified into two groups: homologs or prototypes vertebrate novel (Ciona-specific) neuropeptides. We have also cognate receptors these peptides. In particular, we elucidated multiple Ciona-specific by combination machine learning system experimental validation specific interaction predicted neuropeptide-receptor pairs, verified unprecedented phylogenies Moreover, several were found play major roles regulation ovarian follicle development. tachykinin facilitates growth vitellogenic follicles via up-regulation enzymatic activities proteases. vasopressin stimulates oocyte maturation ovulation maturation-promoting factor- matrix metalloproteinase-directed collagen degradation, respectively. cholecystokinin triggers receptor tyrosine kinase signaling subsequent activation metalloproteinase. studies revealed neuropeptidergic plays growth, maturation, Ciona, thus paving way biological evolutionary processes various

Language: Английский

Citations

8