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

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...

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Autores principales: Da Fonte, Dillon F., Martyniuk, Chris J., Xing, Lei, Trudeau, Vance L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5845582/
https://www.ncbi.nlm.nih.gov/pubmed/29559953
http://dx.doi.org/10.3389/fendo.2018.00068
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author Da Fonte, Dillon F.
Martyniuk, Chris J.
Xing, Lei
Trudeau, Vance L.
author_facet Da Fonte, Dillon F.
Martyniuk, Chris J.
Xing, Lei
Trudeau, Vance L.
author_sort Da Fonte, Dillon F.
collection PubMed
description 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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spelling pubmed-58455822018-03-20 Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro Da Fonte, Dillon F. Martyniuk, Chris J. Xing, Lei Trudeau, Vance L. Front Endocrinol (Lausanne) Endocrinology 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. Frontiers Media S.A. 2018-03-06 /pmc/articles/PMC5845582/ /pubmed/29559953 http://dx.doi.org/10.3389/fendo.2018.00068 Text en Copyright © 2018 Da Fonte, Martyniuk, Xing and Trudeau. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Endocrinology
Da Fonte, Dillon F.
Martyniuk, Chris J.
Xing, Lei
Trudeau, Vance L.
Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro
title Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro
title_full Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro
title_fullStr Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro
title_full_unstemmed Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro
title_short Secretoneurin A Directly Regulates the Proteome of Goldfish Radial Glial Cells In Vitro
title_sort secretoneurin a directly regulates the proteome of goldfish radial glial cells in vitro
topic Endocrinology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5845582/
https://www.ncbi.nlm.nih.gov/pubmed/29559953
http://dx.doi.org/10.3389/fendo.2018.00068
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