A relaxin-like peptide purified from radial nerves induces oocyte maturation and ovulation in the starfish, Asterina pectinifera

Abstract

Gonad-stimulating substance (GSS) of starfish is the only known invertebrate peptide hormone responsible for final gamete maturation, rendering it functionally analogous to the vertebrate luteinizing hormone (LH). Here, we purified GSS of starfish, Asterina pectinifera, from radial nerves and determined its amino acid sequence. The purified GSS was a heterodimer composed of 2 different peptides, A and B chains, with disulfide cross-linkages. Based on its cysteine motif, starfish GSS was classified as a member of the insulin/insulin-like growth factor (IGF)/relaxin superfamily. The cDNA of GSS encodes a preprohormone sequence with a C peptide between the A and B chains. Phylogenetic analyses revealed that starfish GSS was a relaxin-like peptide. Chemically synthesized GSS induced not only oocyte maturation and ovulation in isolated ovarian fragments, but also unique spawning behavior, followed by release of gametes shortly after the injection. Importantly, the action of the synthetic GSS on oocyte maturation and ovulation was mediated through the production of cAMP by isolated ovarian follicle cells, thereby producing the maturationinducing hormone of this species, 1-methyladenine. In situ hybridization showed the transcription of GSS to occur in the periphery of radial nerves at the side of tube feet. Together, the structure, sequence, and mode of signal transduction strongly suggest that GSS is closely related to the vertebrate relaxin.gonadotropin ͉ gonad-stimulating substance ͉ insulin-like growth factor/relaxin superfamily ͉ 1-methyladenine ͉ in situ hybridization

Effect of Relaxin-Like Gonad-Stimulating Substance on Gamete Shedding and 1-Methyladenine Production in Starfish Ovaries

“…In contrast, GSS-induced 1-MeAde production in isolated follicle cells increased in a dosedependent manner and reached a plateau at concentrations above 2 nM GSS ( Fig. 10.2b ), which agrees with previous reports (Mita et al 1987(Mita et al , 2009 ). Because GSS stimulates follicle cells as a target in starfi sh ovaries ( Hirai and Kanatani 1971 ;Hirai et al 1973 ), it is possible that unknown matter within the ovaries affects GSS action on follicle cells to produce 1-MeAde.…”

“…However, crude GSS inhibits spawning at a high concentration (Kanatani and Shirai 1970 ). Recently, GSS was purifi ed from the radial nerves of the starfi sh Asterina pectinifera and its chemical structure was determined to be a relaxin-like peptide (Mita et al 2009 ). In this chapter, hormonal action of GSS on spawning is described from the aspect of 1-MeAde production within ovaries.…”

SALMFamide salmagundi: The biology of a neuropeptide family in echinoderms

“…Gamete release in starfish is 271 triggered by gonad-stimulating substance (GSS), a neurohormone that is present in starfish radial 272 nerve cords and that is related to the mammalian hormone relaxin [50]. Release of GSS from radial 273 nerve cords can be triggered in vitro by KCl-induced depolarisation and S1 causes dose-dependent 274 inhibition of KCl-induced GSS release [49].…”

Incapacity of 1-Methyladenine Production to Relaxin-Like Gonad-Stimulating Substance in Ca2+-Free Seawater-Treated Starfish Ovarian Follicle Cells

“…Resumption of meiosis in these immature oocytes is induced by 1-MeAde, which is produced by ovarian follicle cells on stimulation by GSS released from radial nerves (Kanatani et al 1969 ;Kanatani 1985 ). Recently, GSS was purifi ed from the radial nerves of the starfi sh Asterina pectinifera and its chemical structure was determined to be a relaxin-like peptide (Mita et al 2009 ). In this chapter, 1-MeAde production in follicle cells as a role of GSS is described from the aspect of signal transduction mode, based on incapacity of follicle cells to produce 1-MeAde after washing with CaFSW.…”