Oocyte Maturation in Starfish

Chiba, Kazuyoshi

doi:10.3390/cells9020476

Cited by 8 publications

(5 citation statements)

References 46 publications

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“…The GSS are known to induce oocyte maturation and ovulation in a two step process, where GSS stimulates the follicle cells to produce 1-methyladenine which subsequently induces resumption of meiosis in the oocyte and about 30 min later this is followed by ovulation ( Chiba, 2020 ). Interestingly, GSS was not found in either the genome nor the extensive transcriptome data from the feather star Anneissia japonica and was similarly not encountered in the transcriptomes of three other crinoids ( Data S1 ).…”

Section: Resultsmentioning

confidence: 99%

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor

Veenstra

2021

PeerJ

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Background Some insulin/IGF-related peptides (irps) stimulate a receptor tyrosine kinase (RTK) that transfers the extracellular hormonal signal into an intracellular response. Other irps, such as relaxin, do not use an RTK, but a G-protein coupled receptor (GPCR). This is unusual since evolutionarily related hormones typically either use the same or paralogous receptors. In arthropods three different irps, i.e. arthropod IGF, gonadulin and Drosophila insulin-like peptide 7 (dilp7), likely evolved from a gene triplication, as in several species genes encoding these three peptides are located next to one another on the same chromosomal fragment. These arthropod irps have homologs in vertebrates, suggesting that the initial gene triplication was perhaps already present in the last common ancestor of deuterostomes and protostomes. It would be interesting to know whether this is indeed so and how insulin might be related to this trio of irps. Methodology Genes encoding irps as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates. Results A similar triplet of genes coding for irps also occurs in some ambulacrarians. Two of these are orthologs of arthropod IGF and dilp7 and the third is likely a gonadulin ortholog. In echinoderms, two novel irps emerged, gonad stimulating substance (GSS) and multinsulin, likely from gene duplications of the IGF and dilp7-like genes respectively. The structures of GSS diverged considerably from IGF, which would suggest they use different receptors from IGF, but no novel irp receptors evolved. If IGF and GSS use different receptors, and the evolution of GSS from a gene duplication of IGF is not associated with the appearance of a novel receptor, while irps are known to use two different types of receptors, the ancestor of GSS and IGF might have acted on both types of receptors while one or both of its descendants act on only one. There are three ambulacrarian GPCRs that have amino acid sequences suggestive of being irp GPCRs, two of these are orthologs of the gonadulin and dilp7 receptors. This suggests that the third might be an IGF receptor, and that by deduction, GSS only acts on the RTK. The evolution of GSS from IGF may represent a pattern, where IGF gene duplications lead to novel genes coding for shorter peptides that activate an RTK. It is likely this is how insulin and the insect neuroendocrine irps evolved independently from IGF. Conclusion The local gene triplication described from arthropods that yielded three genes encoding irps was already present in the last common ancestor of protostomes and deuterostomes. It seems plausible that irps, such as those produced by neuroendocrine cells in the brain of insects and echinoderm GSS evolved independently from IGF and, thus, are not true orthologs, but the result of convergent evolution.

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Section: Resultsmentioning

confidence: 99%

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor

Veenstra

2021

PeerJ

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“…The GSS are known to induce oocyte maturation and ovulation in a two step process, where GSS stimulates the follicle cells to produce 1-methyladenine which subsequently induces resumption of meiosis in the oocyte and about 30 minutes later this is followed by ovulation (Chiba, 2020). Interestingly, GSS was not found in either the genome nor the extensive transcriptome data from the feather star Anneissia japonica and was similarly not encountered in the transcriptomes of three other crinoids (Suppl data).…”

Section: Resultsmentioning

confidence: 99%

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from Insulin-like Growth Factor

Veenstra

2021

Preprint

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Background: Insulin is evolutionarily related to the insulin-like growth factors (IGFs) and like the latter stimulates a receptor tyrosine kinase (RTK) that transfers the extracellular hormonal signal into an intracellular response. Other hormones related to insulin, such as relaxin, do not use an RTK, but a G-protein coupled receptor (GPCR). This is unusual since evolutionarily related hormones typically either use the same or paralogous receptors. In arthropods three different IGF-related peptides likely evolved from a gene triplication, as in several species genes coding these three peptides are located next to one another on the same chromosomal fragment. Of these three hormones one, an IGF-like hormone, acts through an RTK, while the other two use a GPCR. This suggests that the ancestral IGF-like peptide may have used both types of receptors. These arthropod insulin-like peptides have homologs in vertebrates, which suggests that the initial gene triplication was perhaps already present in the last common ancestor of deuterostomes and protostomes. It would be interesting to know whether this is indeed so and to establish how insulin and other insulin-like peptides might be related to this trio of IGF-related hormones. Methodology: Genes coding insulin and related peptides as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates. Results: A similar triplet of genes coding insulin-like peptides is also found in some hemichordates and echinoderms. Two of the three ambulacrarian peptides are orthologs of arthropod IGF and Drosophila insulin-like peptide 7 (dilp7), while the third one looks like an ortholog of the arthropod peptide gonadulin. In echinoderms two novel insulin-like peptides emerged, gonad stimulating substance (GSS) and multinsulin, likely from gene duplications of the IGF and dilp7-like genes respectively. However, no novel receptors for insulin-like peptides evolved. If IGF were to act through both a GPCR and an RTK it would suggest that GSS acts on only one of the two receptors, possibly the RTK. The evolution of GSS from IGF may represent a pattern, where IGF gene duplications lead to novel genes coding shorter peptides that have lost their ability to activate a GPCR. It is likely this is how insulin and the insect neuroendocrine insulin-like peptides evolved independently from IGF. Conclusion: The local gene triplication previously described from arthropods that yielded three genes coding IGF-related peptides was already present in the last common ancestor of protostomes and deuterostomes. It seems plausible that insulin and other insulin-like peptides, such as those produced by neuroendocrine cells in the brain of insects and echinoderm GSS evolved independently from IGF and thus are not true orthologs, but the result of convergent evolution.

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“…cAMP is involved in a variety of cellular activation processes through cAMP-dependent protein kinases and, at least in mammals, it is well established that cAMP maintains the oocyte in meiotic arrest and that reinitiation of meiosis is subsequent to a drop in intraoocyte concentrations of cAMP (see [ 42 ] for review). More specifically in asteroids, a decrease of cAMP is also triggered during oocyte maturation by 1MeAd [ 43 ], which binds to an unidentified receptor to separate subunit of protein G and initiate a cascade that activates the MPF (i.e., CDK1 and Cyclin) and induce GVBD (see [ 44 ] for review).…”

Section: Discussionmentioning

confidence: 99%

Intracellular Pathways of Holothuroid Oocyte Maturation Induced by the Thioredoxin Trx-REES

et al. 2021

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In holothuroids, oocyte maturation is stopped in ovaries at the prophase I stage of meiosis. In natural conditions, the blockage is removed during the spawning by an unknown mechanism. When oocytes are isolated by dissection, the meiotic release can be successfully induced by a natural inducer, the REES (i.e., Rough Extract of Echinoid Spawn) that is used in aquaculture to obtain viable larvae in mass. A thioredoxin has recently been identified in the REES as the molecule responsible for holothuroid oocyte maturation. As a redox-active protein, thioredoxin is thought to reduce target proteins within the oocyte membrane and initiate an intracellular reaction cascade that leads to the unblocking of the oocyte meiosis. Our results allow us to understand additional steps in the intracellular reaction cascade induced by the action of thioredoxin on oocytes. Pharmacological agents known to have activating or inhibiting actions on oocyte maturation have been used (Forskolin, Isobutylmethylxanthine, Hypoxanthine, 6-dimethyaminopurine, Lavendustin, Genistein, Roscovitine, Cycloheximide). The effects of these agents were analysed on oocytes of the holothuroid Holothuria tubulosa incubated with or without REES and were compared to those obtained with another reducing agent, the dithiothreitol. Our results demonstrated that, at the opposite of dithiothreitol-induced oocyte maturation, thioredoxin-induced oocyte maturation is cAMP independent, but dependent of the presence of calcium in the seawater. Both pathways of induction require the activation of protein serine/threonine kinases.

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Oocyte Maturation in Starfish

Cited by 8 publications

References 46 publications

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from Insulin-like Growth Factor

Intracellular Pathways of Holothuroid Oocyte Maturation Induced by the Thioredoxin Trx-REES

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