Reproductive Hormone and Transcriptomic Responses of Pituitary Tissue in Anestrus Gilts Induced by Nutrient Restriction

The onset of estrus is a critical sign of female sexual maturity. The pituitary plays a vital role in this process by the secretion of reproductive hormones. To investigate the effects of nutrient restriction on reproductive function and the underlying mechanisms involved, deep RNA sequencing of pit...

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Veröffentlicht in:PloS one 2015-11, Vol.10 (11), p.e0143219-e0143219
Hauptverfasser: Xu, Shengyu, Wang, Dingyue, Zhou, Dongsheng, Lin, Yan, Che, Lianqiang, Fang, Zhengfeng, Wu, De
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container_title PloS one
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creator Xu, Shengyu
Wang, Dingyue
Zhou, Dongsheng
Lin, Yan
Che, Lianqiang
Fang, Zhengfeng
Wu, De
description The onset of estrus is a critical sign of female sexual maturity. The pituitary plays a vital role in this process by the secretion of reproductive hormones. To investigate the effects of nutrient restriction on reproductive function and the underlying mechanisms involved, deep RNA sequencing of pituitary gland tissue was carried out to determine the differentially expressed genes (DEGs) between gilts in normal estrus, and gilts in which anestrus was induced by nutrient restriction. Gilts which had gone through two estrus cycles were fed a normal (CON, 2.86kg/d, n = 10) or nutrient restricted (NR, 1kg/d, n = 10) diet. The NR gilts experienced another three estrus cycles, but did not express estrus symptoms at the anticipated 6th and 7th cycles. Body weight gain in NR gilts was significantly decreased by nutrient restriction. Gilts were considered as anestrus when blood progesterone concentrations lower than 1.0 ng/mL from three consecutive blood samples were recorded. Circulating concentrations of progesterone (< 1.0 ng/mL vs. 2.1 ng/mL) and estradiol (208.6 ng/mL vs. 371.8 ng/mL) were significantly lower in the NR gilts than in the CON gilts. Between 5,360,000 and 5,370,000 sequence reads per sample from the CON and NR gilts' pituitaries were obtained and mapped to the porcine genome. Analysis of read counts revealed 185 DEGs. Expression of selected genes was validated by the use of quantitative real-time RT-PCR. Bioinformatic analysis identified that the genes identified were enriched in the GO terms "neuroactive ligand-receptor interaction", "GnRH signaling pathway" and "immune response system". Our findings provide a new perspective for understanding the nutrient restriction-induced reproductive impairment at the pituitary transcriptional level, and how this is linked to hormone secretion. Moreover, the transcriptomic changes in anestrus gilts associated with nutrient restriction could be a resource for targeted studies of genes and pathways potentially involved in the regulation of reproductive function and animal health.
doi_str_mv 10.1371/journal.pone.0143219
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The pituitary plays a vital role in this process by the secretion of reproductive hormones. To investigate the effects of nutrient restriction on reproductive function and the underlying mechanisms involved, deep RNA sequencing of pituitary gland tissue was carried out to determine the differentially expressed genes (DEGs) between gilts in normal estrus, and gilts in which anestrus was induced by nutrient restriction. Gilts which had gone through two estrus cycles were fed a normal (CON, 2.86kg/d, n = 10) or nutrient restricted (NR, 1kg/d, n = 10) diet. The NR gilts experienced another three estrus cycles, but did not express estrus symptoms at the anticipated 6th and 7th cycles. Body weight gain in NR gilts was significantly decreased by nutrient restriction. Gilts were considered as anestrus when blood progesterone concentrations lower than 1.0 ng/mL from three consecutive blood samples were recorded. Circulating concentrations of progesterone (&lt; 1.0 ng/mL vs. 2.1 ng/mL) and estradiol (208.6 ng/mL vs. 371.8 ng/mL) were significantly lower in the NR gilts than in the CON gilts. Between 5,360,000 and 5,370,000 sequence reads per sample from the CON and NR gilts' pituitaries were obtained and mapped to the porcine genome. Analysis of read counts revealed 185 DEGs. Expression of selected genes was validated by the use of quantitative real-time RT-PCR. Bioinformatic analysis identified that the genes identified were enriched in the GO terms "neuroactive ligand-receptor interaction", "GnRH signaling pathway" and "immune response system". Our findings provide a new perspective for understanding the nutrient restriction-induced reproductive impairment at the pituitary transcriptional level, and how this is linked to hormone secretion. 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This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Xu et al 2015 Xu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-561f238c6ac5c385b1995b39e32c0cdcc1c79ead5463c05a7159af4af068190b3</citedby><cites>FETCH-LOGICAL-c692t-561f238c6ac5c385b1995b39e32c0cdcc1c79ead5463c05a7159af4af068190b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4651501/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4651501/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26580562$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Shen, Wei</contributor><creatorcontrib>Xu, Shengyu</creatorcontrib><creatorcontrib>Wang, Dingyue</creatorcontrib><creatorcontrib>Zhou, Dongsheng</creatorcontrib><creatorcontrib>Lin, Yan</creatorcontrib><creatorcontrib>Che, Lianqiang</creatorcontrib><creatorcontrib>Fang, Zhengfeng</creatorcontrib><creatorcontrib>Wu, De</creatorcontrib><title>Reproductive Hormone and Transcriptomic Responses of Pituitary Tissue in Anestrus Gilts Induced by Nutrient Restriction</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The onset of estrus is a critical sign of female sexual maturity. The pituitary plays a vital role in this process by the secretion of reproductive hormones. To investigate the effects of nutrient restriction on reproductive function and the underlying mechanisms involved, deep RNA sequencing of pituitary gland tissue was carried out to determine the differentially expressed genes (DEGs) between gilts in normal estrus, and gilts in which anestrus was induced by nutrient restriction. Gilts which had gone through two estrus cycles were fed a normal (CON, 2.86kg/d, n = 10) or nutrient restricted (NR, 1kg/d, n = 10) diet. The NR gilts experienced another three estrus cycles, but did not express estrus symptoms at the anticipated 6th and 7th cycles. Body weight gain in NR gilts was significantly decreased by nutrient restriction. Gilts were considered as anestrus when blood progesterone concentrations lower than 1.0 ng/mL from three consecutive blood samples were recorded. 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metabolism</subject><subject>Physiological aspects</subject><subject>Pituitary</subject><subject>Pituitary gland</subject><subject>Pituitary Gland - chemistry</subject><subject>Pituitary Gland - metabolism</subject><subject>Pituitary hormones</subject><subject>Polymerase chain reaction</subject><subject>Progesterone</subject><subject>Progesterone - blood</subject><subject>Puberty</subject><subject>Reproduction - genetics</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA sequencing</subject><subject>Sex hormones</subject><subject>Sexual maturity</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>Swine</subject><subject>Transcription</subject><subject>Transcriptome</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk19v0zAUxSMEYqPwDRBYQkLw0OI_sZO8IFUTbJUmhkrh1XKcm9ZVGne2M9i3x1mzqUF7QHmI5fzuOTnXvknymuAZYRn5tLWda1Uz29sWZpikjJLiSXJKCkangmL29Gh9krzwfosxZ7kQz5MTKniOuaCnye8l7J2tOh3MDaAL63ZRDqm2QiunWq-d2Qe7MxotwUcnDx7ZGn03oTNBuVu0Mt53gEyL5i344DqPzk0TPFq0URQqVN6ib11wBtrQa8RVtLLty-RZrRoPr4b3JPn59cvq7GJ6eXW-OJtfTrUoaJhyQWrKci2U5prlvCRFwUtWAKMa60prorMCVMVTwTTmKiO8UHWqaixyUuCSTZK3B919Y70ceuYlyVhKs0ywPBKLA1FZtZV7Z3Yxl7TKyLsN69ZSuWB0AzIrKSlBR98sTZVKS8Ux1RRywLXg0Gt9Hty6cgeVjqGdakai4y-t2ci1vZGp4IRjEgU-DALOXnexXXJnvIamUS3Y7u6_eYE5jXEnybt_0MfTDdRaxQCmrW301b2onKcsLbIsz1mkZo9Q8akgnn28EbWJ-6OCj6OCyAT4E9aq814ufiz_n736NWbfH7EbUE3YeNt0_ZXxYzA9gNpZ7x3UD00mWPbzcd8N2c-HHOYjlr05PqCHovuBYH8BDlkNQQ</recordid><startdate>20151118</startdate><enddate>20151118</enddate><creator>Xu, Shengyu</creator><creator>Wang, Dingyue</creator><creator>Zhou, Dongsheng</creator><creator>Lin, Yan</creator><creator>Che, Lianqiang</creator><creator>Fang, Zhengfeng</creator><creator>Wu, De</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20151118</creationdate><title>Reproductive Hormone and Transcriptomic Responses of Pituitary Tissue in Anestrus Gilts Induced by Nutrient Restriction</title><author>Xu, Shengyu ; Wang, Dingyue ; Zhou, Dongsheng ; Lin, Yan ; Che, Lianqiang ; Fang, Zhengfeng ; Wu, De</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-561f238c6ac5c385b1995b39e32c0cdcc1c79ead5463c05a7159af4af068190b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>17β-Estradiol</topic><topic>Analysis</topic><topic>Anestrus</topic><topic>Anestrus - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xu, Shengyu</au><au>Wang, Dingyue</au><au>Zhou, Dongsheng</au><au>Lin, Yan</au><au>Che, Lianqiang</au><au>Fang, Zhengfeng</au><au>Wu, De</au><au>Shen, Wei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reproductive Hormone and Transcriptomic Responses of Pituitary Tissue in Anestrus Gilts Induced by Nutrient Restriction</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-11-18</date><risdate>2015</risdate><volume>10</volume><issue>11</issue><spage>e0143219</spage><epage>e0143219</epage><pages>e0143219-e0143219</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The onset of estrus is a critical sign of female sexual maturity. The pituitary plays a vital role in this process by the secretion of reproductive hormones. To investigate the effects of nutrient restriction on reproductive function and the underlying mechanisms involved, deep RNA sequencing of pituitary gland tissue was carried out to determine the differentially expressed genes (DEGs) between gilts in normal estrus, and gilts in which anestrus was induced by nutrient restriction. Gilts which had gone through two estrus cycles were fed a normal (CON, 2.86kg/d, n = 10) or nutrient restricted (NR, 1kg/d, n = 10) diet. The NR gilts experienced another three estrus cycles, but did not express estrus symptoms at the anticipated 6th and 7th cycles. Body weight gain in NR gilts was significantly decreased by nutrient restriction. Gilts were considered as anestrus when blood progesterone concentrations lower than 1.0 ng/mL from three consecutive blood samples were recorded. Circulating concentrations of progesterone (&lt; 1.0 ng/mL vs. 2.1 ng/mL) and estradiol (208.6 ng/mL vs. 371.8 ng/mL) were significantly lower in the NR gilts than in the CON gilts. Between 5,360,000 and 5,370,000 sequence reads per sample from the CON and NR gilts' pituitaries were obtained and mapped to the porcine genome. Analysis of read counts revealed 185 DEGs. Expression of selected genes was validated by the use of quantitative real-time RT-PCR. Bioinformatic analysis identified that the genes identified were enriched in the GO terms "neuroactive ligand-receptor interaction", "GnRH signaling pathway" and "immune response system". Our findings provide a new perspective for understanding the nutrient restriction-induced reproductive impairment at the pituitary transcriptional level, and how this is linked to hormone secretion. Moreover, the transcriptomic changes in anestrus gilts associated with nutrient restriction could be a resource for targeted studies of genes and pathways potentially involved in the regulation of reproductive function and animal health.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26580562</pmid><doi>10.1371/journal.pone.0143219</doi><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
ispartof PloS one, 2015-11, Vol.10 (11), p.e0143219-e0143219
issn 1932-6203
1932-6203
language eng
recordid cdi_plos_journals_1734277638
source MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry
subjects 17β-Estradiol
Analysis
Anestrus
Anestrus - genetics
Animal diseases
Animal Feed
Animal health
Animals
Blood
Blood circulation
Body weight
Body weight gain
Caloric Restriction
Diet
Dietary restrictions
Education
Estradiol - blood
Estrus
Estrus - genetics
Female
Gene expression
Gene Expression Profiling
Gene Expression Regulation
Gene Ontology
Gene sequencing
Genes
Genetic aspects
Genome
Genomes
Gonadotropin-releasing hormone
Growth hormones
Hogs
Hormones
Immune response
Immune system
Kinases
Laboratories
Molecular Sequence Annotation
Nutrient concentrations
Nutrient cycles
Nutrients
Nutrition
Ovary - metabolism
Physiological aspects
Pituitary
Pituitary gland
Pituitary Gland - chemistry
Pituitary Gland - metabolism
Pituitary hormones
Polymerase chain reaction
Progesterone
Progesterone - blood
Puberty
Reproduction - genetics
Ribonucleic acid
RNA
RNA sequencing
Sex hormones
Sexual maturity
Signal transduction
Signaling
Swine
Transcription
Transcriptome
title Reproductive Hormone and Transcriptomic Responses of Pituitary Tissue in Anestrus Gilts Induced by Nutrient Restriction
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