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

Abstract 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...

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Main Authors: David A. Skerrett-Byrne, Brett Nixon, Elizabeth G. Bromfield, James Breen, Natalie A. Trigg, Simone J. Stanger, Ilana R. Bernstein, Amanda L. Anderson, Tessa Lord, R. John Aitken, Shaun D. Roman, Sarah A. Robertson, John E. Schjenken
Format: Article
Language:English
Published: BMC 2021-10-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-021-07951-1
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author David A. Skerrett-Byrne
Brett Nixon
Elizabeth G. Bromfield
James Breen
Natalie A. Trigg
Simone J. Stanger
Ilana R. Bernstein
Amanda L. Anderson
Tessa Lord
R. John Aitken
Shaun D. Roman
Sarah A. Robertson
John E. Schjenken
author_facet David A. Skerrett-Byrne
Brett Nixon
Elizabeth G. Bromfield
James Breen
Natalie A. Trigg
Simone J. Stanger
Ilana R. Bernstein
Amanda L. Anderson
Tessa Lord
R. John Aitken
Shaun D. Roman
Sarah A. Robertson
John E. Schjenken
author_sort David A. Skerrett-Byrne
collection DOAJ
description Abstract 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.
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spelling doaj.art-627867058628482e8338e8767450f0aa2022-12-21T18:37:06ZengBMCBMC Genomics1471-21642021-10-0122112210.1186/s12864-021-07951-1Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamideDavid A. Skerrett-Byrne0Brett Nixon1Elizabeth G. Bromfield2James Breen3Natalie A. Trigg4Simone J. Stanger5Ilana R. Bernstein6Amanda L. Anderson7Tessa Lord8R. John Aitken9Shaun D. Roman10Sarah A. Robertson11John E. Schjenken12Priority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastlePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastlePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastleThe Robinson Research Institute and Adelaide Medical School, University of AdelaidePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastlePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastlePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastlePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastlePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastlePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastlePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastleThe Robinson Research Institute and Adelaide Medical School, University of AdelaidePriority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Discipline of Biological Sciences, The University of NewcastleAbstract 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.https://doi.org/10.1186/s12864-021-07951-1AcrylamideReproductionReproductive toxicantSeminal vesicleTranscriptomics
spellingShingle David A. Skerrett-Byrne
Brett Nixon
Elizabeth G. Bromfield
James Breen
Natalie A. Trigg
Simone J. Stanger
Ilana R. Bernstein
Amanda L. Anderson
Tessa Lord
R. John Aitken
Shaun D. Roman
Sarah A. Robertson
John E. Schjenken
Transcriptomic analysis of the seminal vesicle response to the reproductive toxicant acrylamide
BMC Genomics
Acrylamide
Reproduction
Reproductive toxicant
Seminal vesicle
Transcriptomics
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 Acrylamide
Reproduction
Reproductive toxicant
Seminal vesicle
Transcriptomics
url https://doi.org/10.1186/s12864-021-07951-1
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