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Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide

BACKGROUND: The seminal vesicles synthesise bioactive factors that support gamete function, modulate the female reproductive tract to promote implantation, and influence developmental programming of offspring phenotype. Despite the significance of the seminal vesicles in reproduction, their biology...

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Autores principales: Skerrett-Byrne, David A., Nixon, Brett, Bromfield, Elizabeth G., Breen, James, Trigg, Natalie A., Stanger, Simone J., Bernstein, Ilana R., Anderson, Amanda L., Lord, Tessa, Aitken, R. John, Roman, Shaun D., Robertson, Sarah A., Schjenken, John E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8499523/
https://www.ncbi.nlm.nih.gov/pubmed/34625024
http://dx.doi.org/10.1186/s12864-021-07951-1
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author Skerrett-Byrne, David A.
Nixon, Brett
Bromfield, Elizabeth G.
Breen, James
Trigg, Natalie A.
Stanger, Simone J.
Bernstein, Ilana R.
Anderson, Amanda L.
Lord, Tessa
Aitken, R. John
Roman, Shaun D.
Robertson, Sarah A.
Schjenken, John E.
author_facet Skerrett-Byrne, David A.
Nixon, Brett
Bromfield, Elizabeth G.
Breen, James
Trigg, Natalie A.
Stanger, Simone J.
Bernstein, Ilana R.
Anderson, Amanda L.
Lord, Tessa
Aitken, R. John
Roman, Shaun D.
Robertson, Sarah A.
Schjenken, John E.
author_sort Skerrett-Byrne, David A.
collection PubMed
description BACKGROUND: The seminal vesicles synthesise bioactive factors that support gamete function, modulate the female reproductive tract to promote implantation, and influence developmental programming of offspring phenotype. Despite the significance of the seminal vesicles in reproduction, their biology remains poorly defined. Here, to advance understanding of seminal vesicle biology, we analyse the mouse seminal vesicle transcriptome under normal physiological conditions and in response to acute exposure to the reproductive toxicant acrylamide. Mice were administered acrylamide (25 mg/kg bw/day) or vehicle control daily for five consecutive days prior to collecting seminal vesicle tissue 72 h following the final injection. RESULTS: A total of 15,304 genes were identified in the seminal vesicles with those encoding secreted proteins amongst the most abundant. In addition to reproductive hormone pathways, functional annotation of the seminal vesicle transcriptome identified cell proliferation, protein synthesis, and cellular death and survival pathways as prominent biological processes. Administration of acrylamide elicited 70 differentially regulated (fold-change ≥1.5 or ≤ 0.67) genes, several of which were orthogonally validated using quantitative PCR. Pathways that initiate gene and protein synthesis to promote cellular survival were prominent amongst the dysregulated pathways. Inflammation was also a key transcriptomic response to acrylamide, with the cytokine, Colony stimulating factor 2 (Csf2) identified as a top-ranked upstream driver and inflammatory mediator associated with recovery of homeostasis. Early growth response (Egr1), C-C motif chemokine ligand 8 (Ccl8), and Collagen, type V, alpha 1 (Col5a1) were also identified amongst the dysregulated genes. Additionally, acrylamide treatment led to subtle changes in the expression of genes that encode proteins secreted by the seminal vesicle, including the complement regulator, Complement factor b (Cfb). CONCLUSIONS: These data add to emerging evidence demonstrating that the seminal vesicles, like other male reproductive tract tissues, are sensitive to environmental insults, and respond in a manner with potential to exert impact on fetal development and later offspring health. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07951-1.
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spelling pubmed-84995232021-10-08 Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide Skerrett-Byrne, David A. Nixon, Brett Bromfield, Elizabeth G. Breen, James Trigg, Natalie A. Stanger, Simone J. Bernstein, Ilana R. Anderson, Amanda L. Lord, Tessa Aitken, R. John Roman, Shaun D. Robertson, Sarah A. Schjenken, John E. BMC Genomics Research BACKGROUND: The seminal vesicles synthesise bioactive factors that support gamete function, modulate the female reproductive tract to promote implantation, and influence developmental programming of offspring phenotype. Despite the significance of the seminal vesicles in reproduction, their biology remains poorly defined. Here, to advance understanding of seminal vesicle biology, we analyse the mouse seminal vesicle transcriptome under normal physiological conditions and in response to acute exposure to the reproductive toxicant acrylamide. Mice were administered acrylamide (25 mg/kg bw/day) or vehicle control daily for five consecutive days prior to collecting seminal vesicle tissue 72 h following the final injection. RESULTS: A total of 15,304 genes were identified in the seminal vesicles with those encoding secreted proteins amongst the most abundant. In addition to reproductive hormone pathways, functional annotation of the seminal vesicle transcriptome identified cell proliferation, protein synthesis, and cellular death and survival pathways as prominent biological processes. Administration of acrylamide elicited 70 differentially regulated (fold-change ≥1.5 or ≤ 0.67) genes, several of which were orthogonally validated using quantitative PCR. Pathways that initiate gene and protein synthesis to promote cellular survival were prominent amongst the dysregulated pathways. Inflammation was also a key transcriptomic response to acrylamide, with the cytokine, Colony stimulating factor 2 (Csf2) identified as a top-ranked upstream driver and inflammatory mediator associated with recovery of homeostasis. Early growth response (Egr1), C-C motif chemokine ligand 8 (Ccl8), and Collagen, type V, alpha 1 (Col5a1) were also identified amongst the dysregulated genes. Additionally, acrylamide treatment led to subtle changes in the expression of genes that encode proteins secreted by the seminal vesicle, including the complement regulator, Complement factor b (Cfb). CONCLUSIONS: These data add to emerging evidence demonstrating that the seminal vesicles, like other male reproductive tract tissues, are sensitive to environmental insults, and respond in a manner with potential to exert impact on fetal development and later offspring health. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07951-1. BioMed Central 2021-10-08 /pmc/articles/PMC8499523/ /pubmed/34625024 http://dx.doi.org/10.1186/s12864-021-07951-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Skerrett-Byrne, David A.
Nixon, Brett
Bromfield, Elizabeth G.
Breen, James
Trigg, Natalie A.
Stanger, Simone J.
Bernstein, Ilana R.
Anderson, Amanda L.
Lord, Tessa
Aitken, R. John
Roman, Shaun D.
Robertson, Sarah A.
Schjenken, John E.
Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide
title Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide
title_full Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide
title_fullStr Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide
title_full_unstemmed Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide
title_short Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide
title_sort transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8499523/
https://www.ncbi.nlm.nih.gov/pubmed/34625024
http://dx.doi.org/10.1186/s12864-021-07951-1
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