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Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle

Audrey Lesage-Padilla, Niamh Forde, Mélanie Poirée, Gareth Healey Orcid Logo, Corinne Giraud-Delville, Pierrette Reinaud, Caroline Eozenou, Anaïs Vitorino Carvalho, Laurent Galio, Mariam Raliou, Jean-François Oudin, Christophe Richard, I. Martin Sheldon, Gilles Charpigny, Pat Lonergan, Olivier Sandra, Martin Sheldon Orcid Logo

PLOS ONE, Volume: 12, Issue: 12, Start page: e0189942

Swansea University Authors: Gareth Healey Orcid Logo, Martin Sheldon Orcid Logo

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DOI (Published version): 10.1371/journal.pone.0189942

Abstract

Intensive selection for milk production has led to reduced reproductive efficiency in high-producing dairy cattle. The impact of intensive milk production on oocyte quality as well as early embryo development has been established but few analyses have addressed this question at the initiation of imp...

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Published in: PLOS ONE
ISSN: 1932-6203
Published: 2017
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URI: https://cronfa.swan.ac.uk/Record/cronfa37796
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The impact of intensive milk production on oocyte quality as well as early embryo development has been established but few analyses have addressed this question at the initiation of implantation, a critical milestone ensuring a successful pregnancy and normal post-natal development. Our study aimed to determine if contrasted maternal metabolism affects the previously described sensory properties of the endometrium to the conceptus in cattle. Following embryo transfer at Day 7 post-oestrus, endometrial caruncular (CAR) and intercaruncular (ICAR) areas were collected at Day 19 from primiparous postpartum Holstein-Friesian cows that were dried-off immediately after parturition (i.e., never milked; DRY) or milked twice daily (LACT). Gene quantification indicated no significant impact of lactation on endometrial expression of transcripts previously reported as conceptus-regulated (PLET1, PTGS2, SOCS6) and interferon-tau stimulated (RSAD2, SOCS1, SOCS3, STAT1) factors or known as female hormone-regulated genes (FOXL2, SCARA5, PTGS2). Compared with LACT cows, DRY cows exhibited mRNA levels with increased expression for FOXL2 transcription factor and decreased expression for oxidative stress-related genes (CAT, SOD1, SOD2). In vivo and in vitro experiments highlighted that neither interferon-tau nor FOXL2 were involved in transcriptional regulation of CAT, SOD1 and SOD2. In addition, our data showed that variations in maternal metabolism had a higher impact on gene expression in ICAR areas. Collectively, our findings prompt the need to fully understand the extent to which modifications in endometrial physiology drive the trajectory of conceptus development from implantation onwards when maternal metabolism is altered.</abstract><type>Journal Article</type><journal>PLOS ONE</journal><volume>12</volume><journalNumber>12</journalNumber><paginationStart>e0189942</paginationStart><publisher/><issnElectronic>1932-6203</issnElectronic><keywords/><publishedDay>27</publishedDay><publishedMonth>12</publishedMonth><publishedYear>2017</publishedYear><publishedDate>2017-12-27</publishedDate><doi>10.1371/journal.pone.0189942</doi><url/><notes/><college>COLLEGE NANME</college><department>Medicine</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>PMSC</DepartmentCode><institution>Swansea University</institution><degreesponsorsfunders>RCUK BBSRC, BB/I017240/1</degreesponsorsfunders><apcterm/><lastEdited>2020-06-18T17:31:36.8421007</lastEdited><Created>2018-01-02T15:45:09.9059174</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Medicine</level></path><authors><author><firstname>Audrey</firstname><surname>Lesage-Padilla</surname><order>1</order></author><author><firstname>Niamh</firstname><surname>Forde</surname><order>2</order></author><author><firstname>M&#xE9;lanie</firstname><surname>Poir&#xE9;e</surname><order>3</order></author><author><firstname>Gareth</firstname><surname>Healey</surname><orcid>0000-0001-9531-1220</orcid><order>4</order></author><author><firstname>Corinne</firstname><surname>Giraud-Delville</surname><order>5</order></author><author><firstname>Pierrette</firstname><surname>Reinaud</surname><order>6</order></author><author><firstname>Caroline</firstname><surname>Eozenou</surname><order>7</order></author><author><firstname>Ana&#xEF;s Vitorino</firstname><surname>Carvalho</surname><order>8</order></author><author><firstname>Laurent</firstname><surname>Galio</surname><order>9</order></author><author><firstname>Mariam</firstname><surname>Raliou</surname><order>10</order></author><author><firstname>Jean-Fran&#xE7;ois</firstname><surname>Oudin</surname><order>11</order></author><author><firstname>Christophe</firstname><surname>Richard</surname><order>12</order></author><author><firstname>I. 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spelling 2020-06-18T17:31:36.8421007 v2 37796 2018-01-02 Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle 5926519f89187489cfd5e1478aa188b1 0000-0001-9531-1220 Gareth Healey Gareth Healey true false ab0f74b794e59cc270c69e63ee1d9748 0000-0001-7902-5558 Martin Sheldon Martin Sheldon true false 2018-01-02 PMSC Intensive selection for milk production has led to reduced reproductive efficiency in high-producing dairy cattle. The impact of intensive milk production on oocyte quality as well as early embryo development has been established but few analyses have addressed this question at the initiation of implantation, a critical milestone ensuring a successful pregnancy and normal post-natal development. Our study aimed to determine if contrasted maternal metabolism affects the previously described sensory properties of the endometrium to the conceptus in cattle. Following embryo transfer at Day 7 post-oestrus, endometrial caruncular (CAR) and intercaruncular (ICAR) areas were collected at Day 19 from primiparous postpartum Holstein-Friesian cows that were dried-off immediately after parturition (i.e., never milked; DRY) or milked twice daily (LACT). Gene quantification indicated no significant impact of lactation on endometrial expression of transcripts previously reported as conceptus-regulated (PLET1, PTGS2, SOCS6) and interferon-tau stimulated (RSAD2, SOCS1, SOCS3, STAT1) factors or known as female hormone-regulated genes (FOXL2, SCARA5, PTGS2). Compared with LACT cows, DRY cows exhibited mRNA levels with increased expression for FOXL2 transcription factor and decreased expression for oxidative stress-related genes (CAT, SOD1, SOD2). In vivo and in vitro experiments highlighted that neither interferon-tau nor FOXL2 were involved in transcriptional regulation of CAT, SOD1 and SOD2. In addition, our data showed that variations in maternal metabolism had a higher impact on gene expression in ICAR areas. Collectively, our findings prompt the need to fully understand the extent to which modifications in endometrial physiology drive the trajectory of conceptus development from implantation onwards when maternal metabolism is altered. Journal Article PLOS ONE 12 12 e0189942 1932-6203 27 12 2017 2017-12-27 10.1371/journal.pone.0189942 COLLEGE NANME Medicine COLLEGE CODE PMSC Swansea University RCUK BBSRC, BB/I017240/1 2020-06-18T17:31:36.8421007 2018-01-02T15:45:09.9059174 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Audrey Lesage-Padilla 1 Niamh Forde 2 Mélanie Poirée 3 Gareth Healey 0000-0001-9531-1220 4 Corinne Giraud-Delville 5 Pierrette Reinaud 6 Caroline Eozenou 7 Anaïs Vitorino Carvalho 8 Laurent Galio 9 Mariam Raliou 10 Jean-François Oudin 11 Christophe Richard 12 I. Martin Sheldon 13 Gilles Charpigny 14 Pat Lonergan 15 Olivier Sandra 16 Martin Sheldon 0000-0001-7902-5558 17 0037796-02022018133027.pdf 37796.pdf 2018-02-02T13:30:27.1900000 Output 4449763 application/pdf Version of Record true 2018-02-02T00:00:00.0000000 Released under the terms of a Creative Commons Attribution License (CC-BY). true eng
title Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle
spellingShingle Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle
Gareth Healey
Martin Sheldon
title_short Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle
title_full Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle
title_fullStr Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle
title_full_unstemmed Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle
title_sort Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle
author_id_str_mv 5926519f89187489cfd5e1478aa188b1
ab0f74b794e59cc270c69e63ee1d9748
author_id_fullname_str_mv 5926519f89187489cfd5e1478aa188b1_***_Gareth Healey
ab0f74b794e59cc270c69e63ee1d9748_***_Martin Sheldon
author Gareth Healey
Martin Sheldon
author2 Audrey Lesage-Padilla
Niamh Forde
Mélanie Poirée
Gareth Healey
Corinne Giraud-Delville
Pierrette Reinaud
Caroline Eozenou
Anaïs Vitorino Carvalho
Laurent Galio
Mariam Raliou
Jean-François Oudin
Christophe Richard
I. Martin Sheldon
Gilles Charpigny
Pat Lonergan
Olivier Sandra
Martin Sheldon
format Journal article
container_title PLOS ONE
container_volume 12
container_issue 12
container_start_page e0189942
publishDate 2017
institution Swansea University
issn 1932-6203
doi_str_mv 10.1371/journal.pone.0189942
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
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
document_store_str 1
active_str 0
description Intensive selection for milk production has led to reduced reproductive efficiency in high-producing dairy cattle. The impact of intensive milk production on oocyte quality as well as early embryo development has been established but few analyses have addressed this question at the initiation of implantation, a critical milestone ensuring a successful pregnancy and normal post-natal development. Our study aimed to determine if contrasted maternal metabolism affects the previously described sensory properties of the endometrium to the conceptus in cattle. Following embryo transfer at Day 7 post-oestrus, endometrial caruncular (CAR) and intercaruncular (ICAR) areas were collected at Day 19 from primiparous postpartum Holstein-Friesian cows that were dried-off immediately after parturition (i.e., never milked; DRY) or milked twice daily (LACT). Gene quantification indicated no significant impact of lactation on endometrial expression of transcripts previously reported as conceptus-regulated (PLET1, PTGS2, SOCS6) and interferon-tau stimulated (RSAD2, SOCS1, SOCS3, STAT1) factors or known as female hormone-regulated genes (FOXL2, SCARA5, PTGS2). Compared with LACT cows, DRY cows exhibited mRNA levels with increased expression for FOXL2 transcription factor and decreased expression for oxidative stress-related genes (CAT, SOD1, SOD2). In vivo and in vitro experiments highlighted that neither interferon-tau nor FOXL2 were involved in transcriptional regulation of CAT, SOD1 and SOD2. In addition, our data showed that variations in maternal metabolism had a higher impact on gene expression in ICAR areas. Collectively, our findings prompt the need to fully understand the extent to which modifications in endometrial physiology drive the trajectory of conceptus development from implantation onwards when maternal metabolism is altered.
published_date 2017-12-27T03:47:39Z
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