Secretoneurin-A inhibits aromatase B (cyp19a1b) expression in female goldfish (Carassius auratus) radial glial cells

Fonte, Dillon F. Da; Xing, Lixin; Mikwar, Myy; Trudeau, Vance L.

doi:10.1016/j.ygcen.2017.04.014

Cited by 11 publications

(8 citation statements)

References 75 publications

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“…Whether E 2 acted directly on nonapeptide neurons in female gobies was not resolved, as the study did not investigate whether nonapeptide neurons express ERs. Oxt neurons in the POA of goldfish, Carassius auratus , are, at least based on immunohistochemical evidence, direct targets for estrogen actions, as they express the membrane estrogen receptor Gper1 ( 96 ) and are surrounded by radial glia, the only cells in the teleost brain expressing cyp19a1b and capable of producing neuroestrogens ( 136 ). While these studies provide evidence for effects of steroids on nonapeptide systems, future studies are warranted to delineate direct and indirect mechanisms of action, and whether effects are mediated by gonadal steroids and feedback regulation and/or local neurosteroids.…”

Section: Reproductive Function Of Nonapeptides In Teleost Fishesmentioning

confidence: 99%

Reproductive roles of the vasopressin/oxytocin neuropeptide family in teleost fishes

et al. 2022

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

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Section: Reproductive Function Of Nonapeptides In Teleost Fishesmentioning

confidence: 99%

Reproductive roles of the vasopressin/oxytocin neuropeptide family in teleost fishes

et al. 2022

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“…These proteins are lost when RGCs differentiate into neurons. Moreover, SNa decreases the expression of aromatase B ( cyp19a1b ) in RGCs in vivo and in vitro in a dose-dependent manner ( 16 ). Taken together, these data suggest that SNa downregulates some of the genes related to the progenitor-like characteristics of this cell type.…”

Section: Discussionmentioning

confidence: 99%

“…We previously reported on the close neuroanatomical relationship between the soma of secretoneurin A (SNa)-immunoreactive magnocellular preoptic neurons and RGCs along the third ventricle in goldfish ( 16 ). The neuropeptide SN is generated from endoproteolytic processing of its precursor protein secretogranin II (SgII) and has well-established functions in endocrine, nervous, and immune systems ( 17 , 18 ).…”

Section: Introductionmentioning

confidence: 99%

“…Currently, there are two known SgII paralogs, SgIIa and SgIIb, that likely arose from the genome duplication events in teleost fish, and these paralogs produce SNa and SNb peptides, respectively ( 19 ). Both in vivo and in vitro , SNa reduces cyp19a1b mRNA levels in goldfish RGCs, implicating SNa in the control of neuroestrogen production ( 16 ). Furthermore, data from transcriptome sequencing of cultured goldfish RGCs revealed that gene networks related to immune responses and CNS physiology were responsive to 1,000 nM SNa ( 15 ).…”

Section: Introductionmentioning

confidence: 99%

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Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro

et al. 2018

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Radial glial cells (RGCs) are the main macroglia in the teleost brain and have established roles in neurogenesis and neurosteroidogenesis. They are the only brain cell type expressing aromatase B (cyp19a1b), the enzyme that synthesizes estrogens from androgen precursors. There are few studies on the regulation of RGC functions, but our previous investigations demonstrated that dopamine stimulates cyp19a1b expression in goldfish RGCs, while secretoneurin A (SNa) inhibits the expression of this enzyme. Here, we determine the range of proteins and cellular processes responsive to SNa treatments in these steroidogenic cells. The focus here is on SNa, because this peptide is derived from selective processing of secretogranin II in magnocellular cells embedded within the RGC-rich preoptic nucleus. Primary cultures of RGCs were treated (24 h) with 10, 100, or 1,000 nM SNa. By using isobaric tagging for relative and absolute quantitation and a Hybrid Quadrupole Obritrap Mass Spectrometry system, a total of 1,363 unique proteins were identified in RGCs, and 609 proteins were significantly regulated by SNa at one or more concentrations. Proteins that showed differential expression with all three concentrations of SNa included H1 histone, glutamyl-prolyl-tRNA synthetase, Rho GDP dissociation inhibitor γ, vimentin A2, and small nuclear ribonucleoprotein-associated protein. At 10, 100, and 1,000 nM SNa, there were 5, 195, and 489 proteins that were downregulated, respectively, whereas the number of upregulated proteins were 72, 44, and 51, respectively. Subnetwork enrichment analysis of differentially regulated proteins revealed that processes such as actin organization, cytoskeleton organization and biogenesis, apoptosis, mRNA processing, RNA splicing, translation, cell growth, and proliferation are regulated by SNa based on the proteomic response. Moreover, we observed that, at the low concentration of SNa, there was an increase in the abundance of proteins involved in cell growth, proliferation, and migration, whereas higher concentration of SNa appeared to downregulate proteins involved in these processes, indicating a dose-dependent proteome response. At the highest concentration of SNa, proteins linked to the etiology of diseases of the central nervous system (brain injuries, Alzheimer disease, Parkinson’s disease, cerebral infraction, brain ischemia) were also differentially regulated. These data implicate SNa in the control of cell proliferation and neurogenesis.

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“…Radial glial cells are the main macroglia and have established roles in neuroesgtogen synthesis as the only site for aromatase B expression in the teleost brain, a characteristic linked to neurogenesis (5). Their previous study indicated that SNa inhibits the expression of aromatase B that converts estrogens from androgen in RGCs (6). The new results based on transcriptomic analysis suggest additional roles for SNa in the control of cell proliferation and neurogenesis.…”

Section: Neurosteroidsmentioning

confidence: 96%

Editorial: Steroids and the Brain

2020

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Secretoneurin-A inhibits aromatase B (cyp19a1b) expression in female goldfish (Carassius auratus) radial glial cells

Cited by 11 publications

References 75 publications

Reproductive roles of the vasopressin/oxytocin neuropeptide family in teleost fishes

Reproductive roles of the vasopressin/oxytocin neuropeptide family in teleost fishes

Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro

Editorial: Steroids and the Brain

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