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Maternal energy insufficiency affects testicular development of the offspring in a swine model
We determined the effects of insufficient maternal energy on testicular development in offspring in a swine model. Thirty-six sows were divided into control (CON) and low-energy diet (LE) groups during gestation. We observed that the number of Sertoli, germ, and Leydig cells in the offspring of the...
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Published in: | Scientific reports 2019-10, Vol.9 (1), p.14533-15, Article 14533 |
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creator | Lin, Yan Xu, Xue-Yu Wu, De Lin, Hao Fang, Zheng-Feng Feng, Bin Xu, Sheng-Yu Che, Lian-Qiang Li, Jian Zhuo, Yong Wu, Cai-Mei Zhang, Jun-Jie Dong, Hong-Jun |
description | We determined the effects of insufficient maternal energy on testicular development in offspring in a swine model. Thirty-six sows were divided into control (CON) and low-energy diet (LE) groups during gestation. We observed that the number of Sertoli, germ, and Leydig cells in the offspring of the CON group were significantly higher than those in the LE group at 28 and 120 d after birth. Furthermore, the percentage of apoptotic testis cells was significantly higher in the offspring of the LE group than in the CON group. Transcriptome analysis of differentially expressed mRNAs and long noncoding RNAs in offspring testes indicated that these RNAs were mainly involved in lipid metabolism, apoptosis, cell proliferation, and some pivotal regulatory pathways. Results revealed that AMPK–PI3K–mTOR, MAPK, and oxidative phosphorylation signaling pathways play an important role in mediating the programming effect of insufficient maternal energy on testicular development, and that this effect occurs mainly at an early stage in life. mRNA and protein expression analyses confirmed the importance of certain signaling pathways in the regulation of testicular development. This study provides insights into the influence and possible mechanism underlying the effect of inadequate maternal energy intake on testicular development in the offspring. |
doi_str_mv | 10.1038/s41598-019-51041-y |
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Thirty-six sows were divided into control (CON) and low-energy diet (LE) groups during gestation. We observed that the number of Sertoli, germ, and Leydig cells in the offspring of the CON group were significantly higher than those in the LE group at 28 and 120 d after birth. Furthermore, the percentage of apoptotic testis cells was significantly higher in the offspring of the LE group than in the CON group. Transcriptome analysis of differentially expressed mRNAs and long noncoding RNAs in offspring testes indicated that these RNAs were mainly involved in lipid metabolism, apoptosis, cell proliferation, and some pivotal regulatory pathways. Results revealed that AMPK–PI3K–mTOR, MAPK, and oxidative phosphorylation signaling pathways play an important role in mediating the programming effect of insufficient maternal energy on testicular development, and that this effect occurs mainly at an early stage in life. mRNA and protein expression analyses confirmed the importance of certain signaling pathways in the regulation of testicular development. This study provides insights into the influence and possible mechanism underlying the effect of inadequate maternal energy intake on testicular development in the offspring.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-019-51041-y</identifier><identifier>PMID: 31601864</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>1-Phosphatidylinositol 3-kinase ; 13/2 ; 13/51 ; 38/43 ; 631/1647/2217/2218 ; 631/443/494 ; Animal Nutritional Physiological Phenomena ; Animals ; Apoptosis ; Birth weight ; Body Weight ; Caloric Restriction ; Cell Proliferation ; Computational Biology ; Energy ; Energy Intake ; Female ; Gene expression ; Gene Expression Profiling ; Gene Library ; Gestation ; Humanities and Social Sciences ; Laboratories ; Leydig cells ; Leydig Cells - metabolism ; Lipid Metabolism ; Male ; MAP kinase ; Maternal Nutritional Physiological Phenomena ; Metabolism ; multidisciplinary ; Nutrient deficiency ; Nutrition research ; Offspring ; Oxidative phosphorylation ; Phosphorylation ; Pregnancy ; Pregnancy, Animal ; Puberty ; RNA, Messenger - metabolism ; Science ; Science (multidisciplinary) ; Sertoli Cells - metabolism ; Signal Transduction ; Swine ; Testes ; Testis - embryology ; Testis - growth & development ; TOR protein ; Transcriptome</subject><ispartof>Scientific reports, 2019-10, Vol.9 (1), p.14533-15, Article 14533</ispartof><rights>The Author(s) 2019</rights><rights>2019. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c540t-3f1f4afd3656f5116a80930dccca3c9387682a53dbfed9e7b072fac49f8c88f3</citedby><cites>FETCH-LOGICAL-c540t-3f1f4afd3656f5116a80930dccca3c9387682a53dbfed9e7b072fac49f8c88f3</cites><orcidid>0000-0002-1712-0047</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2303724360/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2303724360?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31601864$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lin, Yan</creatorcontrib><creatorcontrib>Xu, Xue-Yu</creatorcontrib><creatorcontrib>Wu, De</creatorcontrib><creatorcontrib>Lin, Hao</creatorcontrib><creatorcontrib>Fang, Zheng-Feng</creatorcontrib><creatorcontrib>Feng, Bin</creatorcontrib><creatorcontrib>Xu, Sheng-Yu</creatorcontrib><creatorcontrib>Che, Lian-Qiang</creatorcontrib><creatorcontrib>Li, Jian</creatorcontrib><creatorcontrib>Zhuo, Yong</creatorcontrib><creatorcontrib>Wu, Cai-Mei</creatorcontrib><creatorcontrib>Zhang, Jun-Jie</creatorcontrib><creatorcontrib>Dong, Hong-Jun</creatorcontrib><title>Maternal energy insufficiency affects testicular development of the offspring in a swine model</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>We determined the effects of insufficient maternal energy on testicular development in offspring in a swine model. Thirty-six sows were divided into control (CON) and low-energy diet (LE) groups during gestation. We observed that the number of Sertoli, germ, and Leydig cells in the offspring of the CON group were significantly higher than those in the LE group at 28 and 120 d after birth. Furthermore, the percentage of apoptotic testis cells was significantly higher in the offspring of the LE group than in the CON group. Transcriptome analysis of differentially expressed mRNAs and long noncoding RNAs in offspring testes indicated that these RNAs were mainly involved in lipid metabolism, apoptosis, cell proliferation, and some pivotal regulatory pathways. Results revealed that AMPK–PI3K–mTOR, MAPK, and oxidative phosphorylation signaling pathways play an important role in mediating the programming effect of insufficient maternal energy on testicular development, and that this effect occurs mainly at an early stage in life. mRNA and protein expression analyses confirmed the importance of certain signaling pathways in the regulation of testicular development. This study provides insights into the influence and possible mechanism underlying the effect of inadequate maternal energy intake on testicular development in the offspring.</description><subject>1-Phosphatidylinositol 3-kinase</subject><subject>13/2</subject><subject>13/51</subject><subject>38/43</subject><subject>631/1647/2217/2218</subject><subject>631/443/494</subject><subject>Animal Nutritional Physiological Phenomena</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Birth weight</subject><subject>Body Weight</subject><subject>Caloric Restriction</subject><subject>Cell Proliferation</subject><subject>Computational Biology</subject><subject>Energy</subject><subject>Energy Intake</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Library</subject><subject>Gestation</subject><subject>Humanities and Social Sciences</subject><subject>Laboratories</subject><subject>Leydig cells</subject><subject>Leydig Cells - metabolism</subject><subject>Lipid Metabolism</subject><subject>Male</subject><subject>MAP kinase</subject><subject>Maternal Nutritional Physiological Phenomena</subject><subject>Metabolism</subject><subject>multidisciplinary</subject><subject>Nutrient deficiency</subject><subject>Nutrition research</subject><subject>Offspring</subject><subject>Oxidative phosphorylation</subject><subject>Phosphorylation</subject><subject>Pregnancy</subject><subject>Pregnancy, Animal</subject><subject>Puberty</subject><subject>RNA, Messenger - metabolism</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Sertoli Cells - metabolism</subject><subject>Signal Transduction</subject><subject>Swine</subject><subject>Testes</subject><subject>Testis - embryology</subject><subject>Testis - growth & development</subject><subject>TOR protein</subject><subject>Transcriptome</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNp9kU9PFTEUxRuDEYJ8ARemiRs2g_07025MCFEhwbhhbdPXuX2UzLTPdgYy397CICALu7lN-run596D0AdKTijh6nMRVGrVEKobSYmgzfIGHTAiZMM4Y3sv7vvoqJQbUo9kWlD9Du1z2hKqWnGAfv2wE-RoBwwR8nbBIZbZ--ACRLdg6z24qeAJyhTcPNiMe7iFIe1GiBNOHk_XUIsvuxzitnZji8tdiIDH1MPwHr31dihw9FgP0dW3r1dn583lz-8XZ6eXjZOCTA331Avre97K1ktKW6uI5qR3zlnuNFddq5iVvN946DV0G9Ixb53QXjmlPD9EX1bZ3bwZoXfVW7aDqZ5GmxeTbDD_vsRwbbbp1rSd6jjXVeD4USCn33Md1oyhOBgGGyHNxTBOJBGKaV7RT6_QmzTfb_CB4h0TvCWVYivlciolg38yQ4m5D9CsAZoaoHkI0Cy16ePLMZ5a_sZVAb4C67ohP__9H9k_CgupIA</recordid><startdate>20191010</startdate><enddate>20191010</enddate><creator>Lin, Yan</creator><creator>Xu, Xue-Yu</creator><creator>Wu, De</creator><creator>Lin, Hao</creator><creator>Fang, Zheng-Feng</creator><creator>Feng, Bin</creator><creator>Xu, Sheng-Yu</creator><creator>Che, Lian-Qiang</creator><creator>Li, Jian</creator><creator>Zhuo, Yong</creator><creator>Wu, Cai-Mei</creator><creator>Zhang, Jun-Jie</creator><creator>Dong, Hong-Jun</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1712-0047</orcidid></search><sort><creationdate>20191010</creationdate><title>Maternal energy insufficiency affects testicular development of the offspring in a swine model</title><author>Lin, Yan ; Xu, Xue-Yu ; Wu, De ; Lin, Hao ; Fang, Zheng-Feng ; Feng, Bin ; Xu, Sheng-Yu ; Che, Lian-Qiang ; Li, Jian ; Zhuo, Yong ; Wu, Cai-Mei ; Zhang, Jun-Jie ; Dong, Hong-Jun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c540t-3f1f4afd3656f5116a80930dccca3c9387682a53dbfed9e7b072fac49f8c88f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>1-Phosphatidylinositol 3-kinase</topic><topic>13/2</topic><topic>13/51</topic><topic>38/43</topic><topic>631/1647/2217/2218</topic><topic>631/443/494</topic><topic>Animal Nutritional Physiological Phenomena</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Birth weight</topic><topic>Body Weight</topic><topic>Caloric Restriction</topic><topic>Cell Proliferation</topic><topic>Computational Biology</topic><topic>Energy</topic><topic>Energy Intake</topic><topic>Female</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Library</topic><topic>Gestation</topic><topic>Humanities and Social Sciences</topic><topic>Laboratories</topic><topic>Leydig cells</topic><topic>Leydig Cells - metabolism</topic><topic>Lipid Metabolism</topic><topic>Male</topic><topic>MAP kinase</topic><topic>Maternal Nutritional Physiological Phenomena</topic><topic>Metabolism</topic><topic>multidisciplinary</topic><topic>Nutrient deficiency</topic><topic>Nutrition research</topic><topic>Offspring</topic><topic>Oxidative phosphorylation</topic><topic>Phosphorylation</topic><topic>Pregnancy</topic><topic>Pregnancy, Animal</topic><topic>Puberty</topic><topic>RNA, Messenger - metabolism</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Sertoli Cells - metabolism</topic><topic>Signal Transduction</topic><topic>Swine</topic><topic>Testes</topic><topic>Testis - embryology</topic><topic>Testis - growth & development</topic><topic>TOR protein</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lin, Yan</creatorcontrib><creatorcontrib>Xu, Xue-Yu</creatorcontrib><creatorcontrib>Wu, De</creatorcontrib><creatorcontrib>Lin, Hao</creatorcontrib><creatorcontrib>Fang, Zheng-Feng</creatorcontrib><creatorcontrib>Feng, Bin</creatorcontrib><creatorcontrib>Xu, Sheng-Yu</creatorcontrib><creatorcontrib>Che, Lian-Qiang</creatorcontrib><creatorcontrib>Li, Jian</creatorcontrib><creatorcontrib>Zhuo, Yong</creatorcontrib><creatorcontrib>Wu, Cai-Mei</creatorcontrib><creatorcontrib>Zhang, Jun-Jie</creatorcontrib><creatorcontrib>Dong, Hong-Jun</creatorcontrib><collection>Springer_OA刊</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest_Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Science Database (ProQuest)</collection><collection>Biological Science Database</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lin, Yan</au><au>Xu, Xue-Yu</au><au>Wu, De</au><au>Lin, Hao</au><au>Fang, Zheng-Feng</au><au>Feng, Bin</au><au>Xu, Sheng-Yu</au><au>Che, Lian-Qiang</au><au>Li, Jian</au><au>Zhuo, Yong</au><au>Wu, Cai-Mei</au><au>Zhang, Jun-Jie</au><au>Dong, Hong-Jun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Maternal energy insufficiency affects testicular development of the offspring in a swine model</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2019-10-10</date><risdate>2019</risdate><volume>9</volume><issue>1</issue><spage>14533</spage><epage>15</epage><pages>14533-15</pages><artnum>14533</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>We determined the effects of insufficient maternal energy on testicular development in offspring in a swine model. Thirty-six sows were divided into control (CON) and low-energy diet (LE) groups during gestation. We observed that the number of Sertoli, germ, and Leydig cells in the offspring of the CON group were significantly higher than those in the LE group at 28 and 120 d after birth. Furthermore, the percentage of apoptotic testis cells was significantly higher in the offspring of the LE group than in the CON group. Transcriptome analysis of differentially expressed mRNAs and long noncoding RNAs in offspring testes indicated that these RNAs were mainly involved in lipid metabolism, apoptosis, cell proliferation, and some pivotal regulatory pathways. Results revealed that AMPK–PI3K–mTOR, MAPK, and oxidative phosphorylation signaling pathways play an important role in mediating the programming effect of insufficient maternal energy on testicular development, and that this effect occurs mainly at an early stage in life. mRNA and protein expression analyses confirmed the importance of certain signaling pathways in the regulation of testicular development. This study provides insights into the influence and possible mechanism underlying the effect of inadequate maternal energy intake on testicular development in the offspring.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31601864</pmid><doi>10.1038/s41598-019-51041-y</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-1712-0047</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 1-Phosphatidylinositol 3-kinase 13/2 13/51 38/43 631/1647/2217/2218 631/443/494 Animal Nutritional Physiological Phenomena Animals Apoptosis Birth weight Body Weight Caloric Restriction Cell Proliferation Computational Biology Energy Energy Intake Female Gene expression Gene Expression Profiling Gene Library Gestation Humanities and Social Sciences Laboratories Leydig cells Leydig Cells - metabolism Lipid Metabolism Male MAP kinase Maternal Nutritional Physiological Phenomena Metabolism multidisciplinary Nutrient deficiency Nutrition research Offspring Oxidative phosphorylation Phosphorylation Pregnancy Pregnancy, Animal Puberty RNA, Messenger - metabolism Science Science (multidisciplinary) Sertoli Cells - metabolism Signal Transduction Swine Testes Testis - embryology Testis - growth & development TOR protein Transcriptome |
title | Maternal energy insufficiency affects testicular development of the offspring in a swine model |
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