Dataset Information

Involvement of Membrane Progestin Receptor Beta (mPR?/Paqr8) in Sex Pheromone Progestin-Induced Expression of Luteinizing Hormone in the Pituitary of Male Chinese Black Sleeper (Bostrychus Sinensis).

ABSTRACT: Our previous studies showed that 17?, 20?-dihydroxy-4-pregnen-3-one (DHP) acted as a sex pheromone to induce reproductive success in Chinese black sleeper (Bostrychus sinensis), but its functional mechanism remains unclear. In the present study, we cloned the cDNAs of the gonadotropin subunits (cg?, fsh?, and lh?), and found that, in exposure to 5 nM DHP, transcript levels of lh? significantly increased in the pituitary at 6 h post exposure; plasma 11-KT levels increased at 24 h post exposure in mature male fish. In contrast, DHP exposure failed to increase the transcript levels of lh? in the pituitary of immature male fish, suggesting that the responsiveness to DHP depends on reproductive status. Interestingly, expression of progestin and adipoQ receptor 8 (paqr8, also known as mPR?) and progesterone receptor membrane component 2 significantly increased in the olfactory rosette of male fish at late meiosis stage following a co-injection of human chorionic gonadotropin (HCG) and luteinizing hormone releasing hormone-A3 (LHRH-A3), while no increases of other progestin receptors were observed. Moreover, Paqr8 protein was localized in the dendritic knobs of the olfactory sensory neurons, which were activated following the in vivo exposure to DHP. The DHP-induced expression of lh? in pituitary was not inhibited by RU486, an antagonist of nuclear progesterone receptor. Taken together, our results suggested that sex pheromone DHP increased the expression of lh? transcript in the pituitary and plasma 11-KT levels of mature male, important for reproduction; and Paqr8 might be involved in responding to sex pheromone DHP in the olfactory rosette of male B. sinensis.

SUBMITTER: Zhang YT

PROVIDER: S-EPMC6058016 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Publications

Involvement of Membrane Progestin Receptor Beta (mPRβ/Paqr8) in Sex Pheromone Progestin-Induced Expression of Luteinizing Hormone in the Pituitary of Male Chinese Black Sleeper (Bostrychus Sinensis).

Zhang Yu Ting YT Hong Wan Shu WS Liu Dong Teng DT Qiu Heng Tong HT Zhu Yong Y Chen Shi Xi SX

Frontiers in endocrinology 20180718

Our previous studies showed that 17α, 20β-dihydroxy-4-pregnen-3-one (DHP) acted as a sex pheromone to induce reproductive success in Chinese black sleeper (Bostrychus sinensis), but its functional mechanism remains unclear. In the present study, we cloned the cDNAs of the gonadotropin subunits (cgα, fshβ, and lhβ), and found that, in exposure to 5 nM DHP, transcript levels of lhβ significantly increased in the pituitary at 6 h post exposure; plasma 11-KT levels ...[more]

PMID: 30072952

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Project description:Our previous studies suggested that 17α,20β-dihydroxy-4-pregnen-3-one (DHP), an oocyte maturation inducing progestin, also acts as a sex pheromone in Chinese black sleeper Bostrichthys sinensis, a fish species that inhabits intertidal zones and mates and spawns inside a muddy burrow. The electro-olfactogram response to DHP increased during the breeding season. In the present study, we cloned the cDNAs of the nine progestin receptors (pgr, paqr5, 6, 7(a, b), 8, 9, pgrmc1, 2) from B. sinensis, analyzed their tissue distribution, and determined the expression in the olfactory rosette during the reproductive cycle in female and male fish. The deduced amino acid sequences of the nine progestin receptors share high sequence identities with those of other fish species and relatively lower homology with their mammalian counterparts, and phylogenetic analyses classified the nine B. sinensis progestin receptors into their respective progestin receptor groups. Tissue distribution of B. sinensis progestin receptors showed differential expression patterns, but all these nine genes were expressed in the olfactory rosette. Interestingly, paqr5 mRNA was found in the intermediate and basal parts of the olfactory epithelium but not in the central core using in situ hybridization, and its expression level was the highest in the olfactory rosette among the tissues examined. These results suggested Paqr5 may have an important role for transmitting progestin signaling in the olfactory system. The expression levels of paqr7a and paqr7b, pgr and pgrmc2 mRNA peaked around the mid meiotic stage, and that of paqr8 peaked at late meiotic stage in the olfactory rosette in males, while the olfactory expression of paqr5 decreased gradually as spermatogenesis progressed. In contrast, the expression of the progestin receptors did not change significantly during the development of the ovary in the olfactory rosette in females, except that of pgr. Interestingly, the changes of paqr8 expression in the olfactory rosette in males mirrored the changes of plasma DHP levels in females during the reproductive cycle, suggesting the Paqr8 may also be important for deciphering progestin signaling released by female. To our knowledge, this is the first time to demonstrate the presence of all known progestin receptors in a teleost olfactory rosette, and to show different expressions between the males and females during the reproductive cycle. This study provides the first evidence on changes of all purported progestin receptors during a reproductive cycle in teleost olfactory rosette, and suggests that distinct olfactory sensitivities to DHP may be due to the changes and compositions of each progestin receptor in B. sinensis.

Project description:17?-estradiol (E2) is an important sex steroid produced by ovary and brain. In mammals, E2 plays an important role in hypothalamus-pituitary-gonad axis to regulate puberty onset, however, little is known about the functional role of E2 in teleost pituitary. Using prepubertal grass carp as model, three nuclear estrogen receptors (nERs: estrogen receptor alpha, estrogen receptor beta 1, and estrogen receptor beta 2) and two G protein-coupled estrogen receptors (GPER1: GPER1a and GPER1b) were isolated from grass carp pituitary. Tissue distribution analysis indicated that both nERs and GPERs were highly detected in grass carp pituitary, which suggested that E2 should play an important role in grass carp pituitary. Using primary cultured grass carp pituitary cells as model, high-throughput RNA-seq was used to examine the E2-induced differentially expressed genes (DEGs). Transcriptomic analysis showed that E2 could significantly upregulate the expression of 28 genes in grass carp pituitary cells, which were characterized into different functions including reproduction, gonad development, and central nervous system development. Further studies confirmed that E2 could induce luteinizing hormone (LH) and follicle-stimulating hormone (FSH) secretion and mRNA expression in prepubertal grass carp pituitary in vivo and in vitro. In the pituitary, LH and FSH regulation by E2 were mediated by both ER? and GPER1. Apparently, E2-induced LH? and FSH? mRNA expression were mediated by adenylyl cyclase/cAMP/protein kinase A, phospholipase C/inositol 1,4,5-triphosphate/protein kinase C, and Ca2+/calmodulin/CaM-dependent protein kinase II pathways. In addition to LH and FSH, E2 could also induce growth regulation by estrogen in breast cancer 1 (a novel regulator for pituitary development) mRNA expression in grass carp pituitary cells. These results, as a whole, suggested that E2 could play an important role in gonadotropin hormone release and pituitary development in prepubertal grass carp.

Dataset Information

Involvement of Membrane Progestin Receptor Beta (mPR?/Paqr8) in Sex Pheromone Progestin-Induced Expression of Luteinizing Hormone in the Pituitary of Male Chinese Black Sleeper (Bostrychus Sinensis).

Publications

Involvement of Membrane Progestin Receptor Beta (mPRβ/Paqr8) in Sex Pheromone Progestin-Induced Expression of Luteinizing Hormone in the Pituitary of Male Chinese Black Sleeper (<i>Bostrychus Sinensis</i>).

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