Characterization and localization of relaxin-like gonad-stimulating peptide in the crown-of-thorns starfish, Acanthaster cf. solaris

Mita, Masatoshi; Osugi, Tomohiro; Kawada, Toru; Satake, Honoo; Katayama, Hidekazu; Kitamura, Takaya; Miura, Tetsuji; Miura, Chiemi

doi:10.1016/j.ygcen.2022.114107

Cited by 5 publications

(8 citation statements)

References 42 publications

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“…The expression of RGP in the cardiac stomach of starfish has been reported previously based on analysis of tissue extracts for GSS/RGP bioactivity, PCR‐based detection of RGP transcripts, or immunoassays (Haraguchi et al., 2016; Mita & Katayama, 2018, 2022; Mita, Ito, et al., 2009). However, this is the first study to visualize RGP expression in the starfish digestive system using mRNA in situ hybridization and immunohistochemistry.…”

Section: Discussionmentioning

confidence: 99%

Localization of relaxin‐like gonad‐stimulating peptide expression in starfish reveals the gonoducts as a source for its role as a regulator of spawning

González

Lin

et al. 2023

J of Comparative Neurology

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Oocyte maturation and gamete release (spawning) in starfish are triggered by relaxin‐like gonad‐stimulating peptide (RGP), a neuropeptide that was first isolated from the radial nerve cords of these animals. Hitherto, it has generally been assumed that the radial nerve cords are the source of RGP that triggers spawning physiologically. To investigate other sources of RGP, here we report the first comprehensive anatomical analysis of its expression, using both in situ hybridization and immunohistochemistry to map RGP precursor transcripts and RGP, respectively, in the starfish Asterias rubens. Cells expressing RGP precursor transcripts were revealed in the ectoneural epithelium of the radial nerve cords and circumoral nerve ring, arm tips, tube feet, cardiac stomach, pyloric stomach, and, most notably, gonoducts. Using specific antibodies to A. rubens RGP, immunostaining was revealed in cells and/or fibers in the ectoneural region of the radial nerve cords and circumoral nerve ring, tube feet, terminal tentacle and other arm tip‐associated structures, body wall, peristomial membrane, esophagus, cardiac stomach, pyloric stomach, pyloric caeca, and gonoducts. Our discovery that RGP is expressed in the gonoducts of A. rubens proximal to its gonadotropic site of action in the gonads is important because it provides a new perspective on how RGP may act as a gonadotropin in starfish. Thus, we hypothesize that it is the release of RGP from the gonoducts that triggers gamete maturation and spawning in starfish, while RGP produced in other parts of the body may regulate other physiological/behavioral processes.

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Section: Discussionmentioning

confidence: 99%

Localization of relaxin‐like gonad‐stimulating peptide expression in starfish reveals the gonoducts as a source for its role as a regulator of spawning

González

Lin

et al. 2023

J of Comparative Neurology

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“…The chemical structures of RGP have been identified in several species of starfish, Asterias amurensis (Aam-RGP) [23], Asterias rubens (Aru-RGP) [15,24,25], Aphelasterias japonica (Aja-RGP) [26], Astropecten scoparius (Asc-RGP) [27,28], and the crown-of-thorns starfish (COTS) Achanthaster cf. solaris (Aso-RGP) [29][30][31][32] (Figure 2A). Spawning-inducing activities were recognized in chemically synthesized Ppe-RGP, Aam-RGP, Aru-RGP, Aja-RGP, Asc-RGP, and Aso-RGP [19,23,[25][26][27][28]32].…”

Section: Orthologs Of Rgpmentioning

confidence: 99%

“…solaris (Aso-RGP) [29][30][31][32] (Figure 2A). Spawning-inducing activities were recognized in chemically synthesized Ppe-RGP, Aam-RGP, Aru-RGP, Aja-RGP, Asc-RGP, and Aso-RGP [19,23,[25][26][27][28]32]. The class Asteroida is classified into seven orders: Forcipulatida, Paxillosida, Velatida, Valvatida, Spinulosida, Notomyotida, and Brisingida.…”

Section: Orthologs Of Rgpmentioning

confidence: 99%

“…In A. rubens, cells expressing RGP transcripts were revealed in the ectoneural epithelium of the radial nerve cords, the circumoral nerve ring, and the tube feet [25]. Furthermore, an immunohistochemical analysis using RGP-specific antibodies revealed that RGP is distributed not only in the epithelium of the ectoneural region but also in the neuropile of the ectoneural region in the radial nerve cords of crown-of-thorns starfish (COTS) [32]. This suggests that RGP synthesized in the epithelial cells around the radial nerve cords is transported to the ectoneural neuropile regions and accumulates there.…”

Section: Localization Of Rgpmentioning

confidence: 99%

“…Ppe-RGP can induce oocyte maturation and ovulation in ovarian fragments of A. cf. solaris [29,32], A. amurensis [23], A. japonica [26], A. rubens [25], and A. scoparius [27,28]. Although Aam-RGP induces spawning in the A. japonica ovary, Aam-RGP and Aja-RGP are inactive in the P. pectinifera ovary.…”

Section: Species Specificity Of Rgpmentioning

confidence: 99%

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Relaxin-like Gonad-Stimulating Peptides in Asteroidea

Mita

2023

Biomolecules

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Starfish relaxin-like gonad-stimulating peptide (RGP) is the first identified peptide hormone with gonadotropin-like activity in invertebrates. RGP is a heterodimeric peptide, comprising A and B chains with disulfide cross-linkages. Although RGP had been named a gonad-stimulating substance (GSS), the purified peptide is a member of relaxin-type peptide family. Thus, GSS was renamed as RGP. The cDNA of RGP encodes not only the A and B chains, but also signal and C-peptides. After the rgp gene is translated as a precursor, mature RGP is produced by eliminating the signal and C-peptides. Hitherto, twenty-four RGP orthologs have been identified or predicted from starfish in the orders Valvatida, Forcipulatida, Paxillosida, Spinulosida, and Velatida. The molecular evolution of the RGP family is in good accordance with the phylogenetic taxonomy in Asteroidea. Recently, another relaxin-like peptide with gonadotropin-like activity, RLP2, was found in starfish. RGP is mainly present in the radial nerve cords and circumoral nerve rings, but also in the arm tips, the gonoducts, and the coelomocytes. RGP acts on ovarian follicle cells and testicular interstitial cells to induce the production of 1-methyladenine (1-MeAde), a starfish maturation-inducing hormone. RGP-induced 1-MeAde production is accompanied by an increase in intracellular cyclic AMP levels. This suggests that the receptor for RGP (RGPR) is a G protein-coupled receptor (GPCR). Two types of GPCRs, RGPR1 and RGPR2, have been postulated as candidates. Furthermore, 1-MeAde produced by RGP not only induces oocyte maturation, but also induces gamete shedding, possibly by stimulating the secretion of acetylcholine in the ovaries and testes. Thus, RGP plays an important role in starfish reproduction, but its secretion mechanism is still unknown. It has also been revealed that RGP is found in the peripheral adhesive papillae of the brachiolaria arms. However, gonads are not developed in the larvae before metamorphosis. It may be possible to discover new physiological functions of RGP other than gonadotropin-like activity.

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Endocrine regulation of reproductive biology in echinoderms: An evolutionary perspective from closest marine invertebrate relatives to chordates

Wang,

Liu,

Zheng

et al. 2024

Molecular and Cellular Endocrinology

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Characterization and localization of relaxin-like gonad-stimulating peptide in the crown-of-thorns starfish, Acanthaster cf. solaris

Cited by 5 publications

References 42 publications

Localization of relaxin‐like gonad‐stimulating peptide expression in starfish reveals the gonoducts as a source for its role as a regulator of spawning

Localization of relaxin‐like gonad‐stimulating peptide expression in starfish reveals the gonoducts as a source for its role as a regulator of spawning

Relaxin-like Gonad-Stimulating Peptides in Asteroidea

Endocrine regulation of reproductive biology in echinoderms: An evolutionary perspective from closest marine invertebrate relatives to chordates

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