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The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection

Mackenzie J. Dickson, Jeanette V. Bishop, Thomas R. Hansen, Martin Sheldon Orcid Logo, John J. Bromfield Orcid Logo

PLOS ONE, Volume: 17, Issue: 3, Start page: e0265062

Swansea University Author: Martin Sheldon Orcid Logo

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DOI (Published version): 10.1371/journal.pone.0265062

Abstract

Pregnancy induces changes in the transcriptome of the bovine endometrium from 15 days after insemination. However, pregnancy is less likely to occur if cows had a postpartum bacterial infection of the uterus, even after the resolution of disease. We hypothesized that uterine bacterial infection alte...

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ISSN: 1932-6203
Published: Public Library of Science (PLoS) 2022
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To examine the endometrial transcriptomic signature of pregnancy, cows were inseminated 130 days after intrauterine infusion of pathogenic Escherichia coli and Trueperella pyogenes, subsequently endometrium was collected 16 days after insemination for RNA sequencing. We found 171 pregnancy regulated genes in cows 146 days after bacterial infection. When comparing our findings with previous studies that described the endometrial transcriptomic signature of pregnancy in healthy cows, 24 genes were consistently differentially expressed in pregnancy, including MX1, MX2 and STAT1. However, 12 pregnancy regulated genes were found only in the endometrium of healthy cows, including ISG15 and TRANK1. Furthermore, 28 pregnancy regulated genes were found only in the endometrium of cows following bacterial infection and these were associated with altered iNOS, TLR, and IL-7 signaling pathways. Although 94 predicted upstream regulators were conserved amongst the studies, 14 were found only in the endometrium of pregnant healthy cows, and 5 were found only in cows following bacterial infection, including AIRE, NFKBIA, and DUSP1. In conclusion, there were both consistent and discordant features of the endometrial transcriptomic signature of pregnancy 146 days after intrauterine bacterial infusion. These findings imply that there is an essential transcriptomic signature of pregnancy, but that infection induces long-term changes in the endometrium that affect the transcriptomic response to pregnancy.</abstract><type>Journal Article</type><journal>PLOS ONE</journal><volume>17</volume><journalNumber>3</journalNumber><paginationStart>e0265062</paginationStart><paginationEnd/><publisher>Public Library of Science (PLoS)</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint/><issnElectronic>1932-6203</issnElectronic><keywords/><publishedDay>31</publishedDay><publishedMonth>3</publishedMonth><publishedYear>2022</publishedYear><publishedDate>2022-03-31</publishedDate><doi>10.1371/journal.pone.0265062</doi><url/><notes/><college>COLLEGE NANME</college><department>Biomedical Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BMS</DepartmentCode><institution>Swansea University</institution><apcterm>Another institution paid the OA fee</apcterm><funders>Funding: This study was supported by Eunice Kennedy Shriver National Institute of Child Health &amp; Human Development of the National Institutes of Health under Award Number R01HD084316. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. In addition, this work is supported by Animal Health and Production and Animal Products: Animal Reproduction grant no. 2019-05310 from the USDA National Institute of Food and Agriculture. 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spelling 2022-05-13T15:12:32.9406417 v2 59755 2022-04-01 The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection ab0f74b794e59cc270c69e63ee1d9748 0000-0001-7902-5558 Martin Sheldon Martin Sheldon true false 2022-04-01 BMS Pregnancy induces changes in the transcriptome of the bovine endometrium from 15 days after insemination. However, pregnancy is less likely to occur if cows had a postpartum bacterial infection of the uterus, even after the resolution of disease. We hypothesized that uterine bacterial infection alters the endometrial transcriptomic signature of pregnancy after the resolution of disease. To examine the endometrial transcriptomic signature of pregnancy, cows were inseminated 130 days after intrauterine infusion of pathogenic Escherichia coli and Trueperella pyogenes, subsequently endometrium was collected 16 days after insemination for RNA sequencing. We found 171 pregnancy regulated genes in cows 146 days after bacterial infection. When comparing our findings with previous studies that described the endometrial transcriptomic signature of pregnancy in healthy cows, 24 genes were consistently differentially expressed in pregnancy, including MX1, MX2 and STAT1. However, 12 pregnancy regulated genes were found only in the endometrium of healthy cows, including ISG15 and TRANK1. Furthermore, 28 pregnancy regulated genes were found only in the endometrium of cows following bacterial infection and these were associated with altered iNOS, TLR, and IL-7 signaling pathways. Although 94 predicted upstream regulators were conserved amongst the studies, 14 were found only in the endometrium of pregnant healthy cows, and 5 were found only in cows following bacterial infection, including AIRE, NFKBIA, and DUSP1. In conclusion, there were both consistent and discordant features of the endometrial transcriptomic signature of pregnancy 146 days after intrauterine bacterial infusion. These findings imply that there is an essential transcriptomic signature of pregnancy, but that infection induces long-term changes in the endometrium that affect the transcriptomic response to pregnancy. Journal Article PLOS ONE 17 3 e0265062 Public Library of Science (PLoS) 1932-6203 31 3 2022 2022-03-31 10.1371/journal.pone.0265062 COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University Another institution paid the OA fee Funding: This study was supported by Eunice Kennedy Shriver National Institute of Child Health & Human Development of the National Institutes of Health under Award Number R01HD084316. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. In addition, this work is supported by Animal Health and Production and Animal Products: Animal Reproduction grant no. 2019-05310 from the USDA National Institute of Food and Agriculture. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. 2022-05-13T15:12:32.9406417 2022-04-01T12:51:33.4670344 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Mackenzie J. Dickson 1 Jeanette V. Bishop 2 Thomas R. Hansen 3 Martin Sheldon 0000-0001-7902-5558 4 John J. Bromfield 0000-0001-5438-2137 5 59755__23758__e50ef0477f2e4681a06587e9641dea0c.pdf journal.pone.0265062.pdf 2022-04-01T12:55:17.3640721 Output 2087528 application/pdf Version of Record true © 2022 Dickson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License true eng http://creativecommons.org/licenses/by/4.0/
title The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection
spellingShingle The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection
Martin Sheldon
title_short The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection
title_full The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection
title_fullStr The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection
title_full_unstemmed The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection
title_sort The endometrial transcriptomic response to pregnancy is altered in cows after uterine infection
author_id_str_mv ab0f74b794e59cc270c69e63ee1d9748
author_id_fullname_str_mv ab0f74b794e59cc270c69e63ee1d9748_***_Martin Sheldon
author Martin Sheldon
author2 Mackenzie J. Dickson
Jeanette V. Bishop
Thomas R. Hansen
Martin Sheldon
John J. Bromfield
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container_title PLOS ONE
container_volume 17
container_issue 3
container_start_page e0265062
publishDate 2022
institution Swansea University
issn 1932-6203
doi_str_mv 10.1371/journal.pone.0265062
publisher Public Library of Science (PLoS)
college_str Faculty of Medicine, Health and Life Sciences
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hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
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description Pregnancy induces changes in the transcriptome of the bovine endometrium from 15 days after insemination. However, pregnancy is less likely to occur if cows had a postpartum bacterial infection of the uterus, even after the resolution of disease. We hypothesized that uterine bacterial infection alters the endometrial transcriptomic signature of pregnancy after the resolution of disease. To examine the endometrial transcriptomic signature of pregnancy, cows were inseminated 130 days after intrauterine infusion of pathogenic Escherichia coli and Trueperella pyogenes, subsequently endometrium was collected 16 days after insemination for RNA sequencing. We found 171 pregnancy regulated genes in cows 146 days after bacterial infection. When comparing our findings with previous studies that described the endometrial transcriptomic signature of pregnancy in healthy cows, 24 genes were consistently differentially expressed in pregnancy, including MX1, MX2 and STAT1. However, 12 pregnancy regulated genes were found only in the endometrium of healthy cows, including ISG15 and TRANK1. Furthermore, 28 pregnancy regulated genes were found only in the endometrium of cows following bacterial infection and these were associated with altered iNOS, TLR, and IL-7 signaling pathways. Although 94 predicted upstream regulators were conserved amongst the studies, 14 were found only in the endometrium of pregnant healthy cows, and 5 were found only in cows following bacterial infection, including AIRE, NFKBIA, and DUSP1. In conclusion, there were both consistent and discordant features of the endometrial transcriptomic signature of pregnancy 146 days after intrauterine bacterial infusion. These findings imply that there is an essential transcriptomic signature of pregnancy, but that infection induces long-term changes in the endometrium that affect the transcriptomic response to pregnancy.
published_date 2022-03-31T04:17:18Z
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