Maternal low-protein diet affects epigenetic regulation of hepatic mitochondrial DNA transcription in a sex-specific manner in newborn piglets associated with GR binding to its promoter
Mitochondrial oxidative phosphorylation (OXPHOS) plays an important role in energy homeostasis by controlling electron transfer and ATP generation. Maternal malnutrition during pregnancy affects mitochondrial (mt) DNA-encoded OXPHOS activity in offspring, yet it is unknown whether epigenetic mechani...
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| description | Mitochondrial oxidative phosphorylation (OXPHOS) plays an important role in energy homeostasis by controlling electron transfer and ATP generation. Maternal malnutrition during pregnancy affects mitochondrial (mt) DNA-encoded OXPHOS activity in offspring, yet it is unknown whether epigenetic mechanism is involved in the transcriptional regulation of mtDNA-encoded OXPHOS genes. In this study, 14 primiparous purebred Meishan sows were fed either standard- (SP, 12% crude protein) or low-protein (LP; 6% crude protein) diets throughout gestation, and the hepatic expression and transcriptional regulation of mtDNA-encoded OXPHOS genes were analyzed in newborn piglets. Maternal low protein diet decreased hepatic mtDNA copy number in males, but not in females. LP male piglets had significantly higher hepatic AMP concentration and low energy charge, which was accompanied by enhanced mRNA expression of NADH dehydrogenase subunits 6, cytochrome c oxidase subunit 1, 2, 3 and cytochrome b, as well as increased cytochrome c oxidase enzyme activity. In contrast, LP female piglets showed significantly lower hepatic AMP concentrations and higher energy charge with no alterations in OXPHOS gene expression. Moreover, LP males demonstrated higher glucocorticoid receptor (GR) binding to the mtDNA promoter compared with SP males, which was accompanied by lower cytosine methylation and hydroxymethylation on mtDNA promoter. Interestingly, opposite changes were seen in females, which showed diminished GR binding and enriched cytosine methylation and hydroxymethylation on mtDNA promoter. These results suggest that maternal low protein diet during pregnancy causes sex-dependent epigenetic alterations in mtDNA-encoded OXPHOS gene expression, possibly GR is involved in mtDNA transcription regulation. |
| doi_str_mv | 10.1371/journal.pone.0063855 |
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Maternal malnutrition during pregnancy affects mitochondrial (mt) DNA-encoded OXPHOS activity in offspring, yet it is unknown whether epigenetic mechanism is involved in the transcriptional regulation of mtDNA-encoded OXPHOS genes. In this study, 14 primiparous purebred Meishan sows were fed either standard- (SP, 12% crude protein) or low-protein (LP; 6% crude protein) diets throughout gestation, and the hepatic expression and transcriptional regulation of mtDNA-encoded OXPHOS genes were analyzed in newborn piglets. Maternal low protein diet decreased hepatic mtDNA copy number in males, but not in females. LP male piglets had significantly higher hepatic AMP concentration and low energy charge, which was accompanied by enhanced mRNA expression of NADH dehydrogenase subunits 6, cytochrome c oxidase subunit 1, 2, 3 and cytochrome b, as well as increased cytochrome c oxidase enzyme activity. In contrast, LP female piglets showed significantly lower hepatic AMP concentrations and higher energy charge with no alterations in OXPHOS gene expression. Moreover, LP males demonstrated higher glucocorticoid receptor (GR) binding to the mtDNA promoter compared with SP males, which was accompanied by lower cytosine methylation and hydroxymethylation on mtDNA promoter. Interestingly, opposite changes were seen in females, which showed diminished GR binding and enriched cytosine methylation and hydroxymethylation on mtDNA promoter. These results suggest that maternal low protein diet during pregnancy causes sex-dependent epigenetic alterations in mtDNA-encoded OXPHOS gene expression, possibly GR is involved in mtDNA transcription regulation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0063855</identifier><identifier>PMID: 23691106</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>5-Methylcytosine - metabolism ; Agriculture ; AMP ; Analysis ; Animals ; Animals, Newborn ; Binding ; Biochemistry ; Biology ; Copy number ; Cytochrome ; Cytochrome b ; Cytochrome-c oxidase ; Cytochromes ; Cytosine ; Cytosine - analogs & derivatives ; Cytosine - metabolism ; Deoxyribonucleic acid ; Diabetes ; Diet ; Dietary Proteins - pharmacology ; DNA ; DNA methylation ; DNA Methylation - drug effects ; DNA, Mitochondrial - genetics ; Electron transfer ; Electron transport ; Electron Transport Complex IV - genetics ; Electron Transport Complex IV - metabolism ; Energy balance ; Energy charge ; Enzymatic activity ; Enzyme activity ; Epigenesis, Genetic - drug effects ; Epigenetic inheritance ; Female ; Females ; Gene expression ; Gene regulation ; Genes ; Genetic research ; Genomes ; Genomics ; Gestation ; Glucocorticoids ; Homeostasis ; Hormones ; Laboratories ; Liver ; Liver - metabolism ; Low protein diet ; Male ; Males ; Malnutrition ; Mammals ; Medicine ; Metabolic syndrome ; Methylation ; Mitochondria ; Mitochondrial DNA ; Mothers ; Musculoskeletal system ; NADH ; NADH dehydrogenase ; Nicotinamide adenine dinucleotide ; Nutrition ; Offspring ; Oxidase ; Oxidases ; Oxidative phosphorylation ; Phosphorylation ; Physiology ; Pregnancy ; Promoter Regions, Genetic - drug effects ; Promoter Regions, Genetic - genetics ; Protein Binding - drug effects ; Proteins ; Pyrimidines ; Receptors, Glucocorticoid - metabolism ; RNA ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Rodents ; Sex ; Sex Characteristics ; Swine ; Systematic review ; Transcription ; Transcription (Genetics) ; Transcription, Genetic - drug effects ; Veterinary Science</subject><ispartof>PloS one, 2013-05, Vol.8 (5), p.e63855</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Jia et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>2013 Jia et al 2013 Jia et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-d267fa029f276c5c7cf16cb1556ec6d08d81abcbe87fd8b82bcfb4b8a8c035003</citedby><cites>FETCH-LOGICAL-c692t-d267fa029f276c5c7cf16cb1556ec6d08d81abcbe87fd8b82bcfb4b8a8c035003</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/PMC3653849/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3653849/$$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/23691106$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Wade, Claire</contributor><creatorcontrib>Jia, Yimin</creatorcontrib><creatorcontrib>Li, Runsheng</creatorcontrib><creatorcontrib>Cong, Rihua</creatorcontrib><creatorcontrib>Yang, Xiaojing</creatorcontrib><creatorcontrib>Sun, Qinwei</creatorcontrib><creatorcontrib>Parvizi, Nahid</creatorcontrib><creatorcontrib>Zhao, Ruqian</creatorcontrib><title>Maternal low-protein diet affects epigenetic regulation of hepatic mitochondrial DNA transcription in a sex-specific manner in newborn piglets associated with GR binding to its promoter</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Mitochondrial oxidative phosphorylation (OXPHOS) plays an important role in energy homeostasis by controlling electron transfer and ATP generation. Maternal malnutrition during pregnancy affects mitochondrial (mt) DNA-encoded OXPHOS activity in offspring, yet it is unknown whether epigenetic mechanism is involved in the transcriptional regulation of mtDNA-encoded OXPHOS genes. In this study, 14 primiparous purebred Meishan sows were fed either standard- (SP, 12% crude protein) or low-protein (LP; 6% crude protein) diets throughout gestation, and the hepatic expression and transcriptional regulation of mtDNA-encoded OXPHOS genes were analyzed in newborn piglets. Maternal low protein diet decreased hepatic mtDNA copy number in males, but not in females. LP male piglets had significantly higher hepatic AMP concentration and low energy charge, which was accompanied by enhanced mRNA expression of NADH dehydrogenase subunits 6, cytochrome c oxidase subunit 1, 2, 3 and cytochrome b, as well as increased cytochrome c oxidase enzyme activity. In contrast, LP female piglets showed significantly lower hepatic AMP concentrations and higher energy charge with no alterations in OXPHOS gene expression. Moreover, LP males demonstrated higher glucocorticoid receptor (GR) binding to the mtDNA promoter compared with SP males, which was accompanied by lower cytosine methylation and hydroxymethylation on mtDNA promoter. Interestingly, opposite changes were seen in females, which showed diminished GR binding and enriched cytosine methylation and hydroxymethylation on mtDNA promoter. These results suggest that maternal low protein diet during pregnancy causes sex-dependent epigenetic alterations in mtDNA-encoded OXPHOS gene expression, possibly GR is involved in mtDNA transcription regulation.</description><subject>5-Methylcytosine - metabolism</subject><subject>Agriculture</subject><subject>AMP</subject><subject>Analysis</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Binding</subject><subject>Biochemistry</subject><subject>Biology</subject><subject>Copy number</subject><subject>Cytochrome</subject><subject>Cytochrome b</subject><subject>Cytochrome-c oxidase</subject><subject>Cytochromes</subject><subject>Cytosine</subject><subject>Cytosine - analogs & derivatives</subject><subject>Cytosine - metabolism</subject><subject>Deoxyribonucleic acid</subject><subject>Diabetes</subject><subject>Diet</subject><subject>Dietary Proteins - pharmacology</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA Methylation - drug effects</subject><subject>DNA, Mitochondrial - genetics</subject><subject>Electron transfer</subject><subject>Electron transport</subject><subject>Electron Transport Complex IV - genetics</subject><subject>Electron Transport Complex IV - metabolism</subject><subject>Energy balance</subject><subject>Energy charge</subject><subject>Enzymatic activity</subject><subject>Enzyme activity</subject><subject>Epigenesis, Genetic - drug effects</subject><subject>Epigenetic inheritance</subject><subject>Female</subject><subject>Females</subject><subject>Gene expression</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genetic research</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Gestation</subject><subject>Glucocorticoids</subject><subject>Homeostasis</subject><subject>Hormones</subject><subject>Laboratories</subject><subject>Liver</subject><subject>Liver - metabolism</subject><subject>Low protein diet</subject><subject>Male</subject><subject>Males</subject><subject>Malnutrition</subject><subject>Mammals</subject><subject>Medicine</subject><subject>Metabolic syndrome</subject><subject>Methylation</subject><subject>Mitochondria</subject><subject>Mitochondrial DNA</subject><subject>Mothers</subject><subject>Musculoskeletal system</subject><subject>NADH</subject><subject>NADH dehydrogenase</subject><subject>Nicotinamide adenine dinucleotide</subject><subject>Nutrition</subject><subject>Offspring</subject><subject>Oxidase</subject><subject>Oxidases</subject><subject>Oxidative phosphorylation</subject><subject>Phosphorylation</subject><subject>Physiology</subject><subject>Pregnancy</subject><subject>Promoter Regions, Genetic - drug effects</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Protein Binding - drug effects</subject><subject>Proteins</subject><subject>Pyrimidines</subject><subject>Receptors, Glucocorticoid - metabolism</subject><subject>RNA</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Rodents</subject><subject>Sex</subject><subject>Sex Characteristics</subject><subject>Swine</subject><subject>Systematic review</subject><subject>Transcription</subject><subject>Transcription (Genetics)</subject><subject>Transcription, Genetic - drug effects</subject><subject>Veterinary Science</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</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>eNqNk11rFDEUhgdRbK3-A9GAIHixazKZyczcFJaqtVAt1I_bkI-T2ZTZZEyybv1p_jsz7bbsgoLMRYbkOe95eZNTFM8JnhPakLdXfh2cGOajdzDHmNG2rh8Uh6Sj5YyVmD7c-T8onsR4hXFNW8YeFwclZR0hmB0Wvz-JBJMOGvxmNgafwDqkLSQkjAGVIoLR9uAgWYUC9OtBJOsd8gYtYRTT7somr5be6WCzzrvPC5SCcFEFO96gWVCgCNezOIKyZqoQzkGYDhxspA8O5R4D5GYiRq9s9qTRxqYlOr1E0jptXY-SRzYT2eMquwxPi0dGDBGebdej4tuH919PPs7OL07PThbnM8W6Ms10yRojcNmZsmGqVo0yhClJ6pqBYhq3uiVCKgltY3Qr21IqIyvZilZhWmNMj4qXt7rj4CPfph45oTWhFesoy8TZLaG9uOJjsCsRfnEvLL_Z8KHnIuSgBuBSK5FvSmsh66qpOiGgqZpOdopWVclI1jredlvLFWgFLmc57Inunzi75L3_ySnLl1t1WeDVViD4H2uI6R-Wt1QvsivrjM9iamWj4ouqacumKfFkZv4XKn8aVlbld2ds3t8reLNXkJkE16kX6xj52ZfL_2cvvu-zr3fYJYghLaMf1tPzivtgdQuq4GMMYO6TI5hPY3OXBp_Ghm_HJpe92E39vuhuTugfBs4YGA</recordid><startdate>20130514</startdate><enddate>20130514</enddate><creator>Jia, Yimin</creator><creator>Li, Runsheng</creator><creator>Cong, Rihua</creator><creator>Yang, Xiaojing</creator><creator>Sun, Qinwei</creator><creator>Parvizi, Nahid</creator><creator>Zhao, Ruqian</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>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130514</creationdate><title>Maternal low-protein diet affects epigenetic regulation of hepatic mitochondrial DNA transcription in a sex-specific manner in newborn piglets associated with GR binding to its promoter</title><author>Jia, Yimin ; Li, Runsheng ; Cong, Rihua ; Yang, Xiaojing ; Sun, Qinwei ; Parvizi, Nahid ; Zhao, Ruqian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-d267fa029f276c5c7cf16cb1556ec6d08d81abcbe87fd8b82bcfb4b8a8c035003</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>5-Methylcytosine - 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Maternal malnutrition during pregnancy affects mitochondrial (mt) DNA-encoded OXPHOS activity in offspring, yet it is unknown whether epigenetic mechanism is involved in the transcriptional regulation of mtDNA-encoded OXPHOS genes. In this study, 14 primiparous purebred Meishan sows were fed either standard- (SP, 12% crude protein) or low-protein (LP; 6% crude protein) diets throughout gestation, and the hepatic expression and transcriptional regulation of mtDNA-encoded OXPHOS genes were analyzed in newborn piglets. Maternal low protein diet decreased hepatic mtDNA copy number in males, but not in females. LP male piglets had significantly higher hepatic AMP concentration and low energy charge, which was accompanied by enhanced mRNA expression of NADH dehydrogenase subunits 6, cytochrome c oxidase subunit 1, 2, 3 and cytochrome b, as well as increased cytochrome c oxidase enzyme activity. In contrast, LP female piglets showed significantly lower hepatic AMP concentrations and higher energy charge with no alterations in OXPHOS gene expression. Moreover, LP males demonstrated higher glucocorticoid receptor (GR) binding to the mtDNA promoter compared with SP males, which was accompanied by lower cytosine methylation and hydroxymethylation on mtDNA promoter. Interestingly, opposite changes were seen in females, which showed diminished GR binding and enriched cytosine methylation and hydroxymethylation on mtDNA promoter. These results suggest that maternal low protein diet during pregnancy causes sex-dependent epigenetic alterations in mtDNA-encoded OXPHOS gene expression, possibly GR is involved in mtDNA transcription regulation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23691106</pmid><doi>10.1371/journal.pone.0063855</doi><tpages>e63855</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-05, Vol.8 (5), p.e63855 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1351346936 |
| source | MEDLINE; PubMed Central(OpenAccess); Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; Free E-Journal (出版社公開部分のみ）; Free Full-Text Journals in Chemistry |
| subjects | 5-Methylcytosine - metabolism Agriculture AMP Analysis Animals Animals, Newborn Binding Biochemistry Biology Copy number Cytochrome Cytochrome b Cytochrome-c oxidase Cytochromes Cytosine Cytosine - analogs & derivatives Cytosine - metabolism Deoxyribonucleic acid Diabetes Diet Dietary Proteins - pharmacology DNA DNA methylation DNA Methylation - drug effects DNA, Mitochondrial - genetics Electron transfer Electron transport Electron Transport Complex IV - genetics Electron Transport Complex IV - metabolism Energy balance Energy charge Enzymatic activity Enzyme activity Epigenesis, Genetic - drug effects Epigenetic inheritance Female Females Gene expression Gene regulation Genes Genetic research Genomes Genomics Gestation Glucocorticoids Homeostasis Hormones Laboratories Liver Liver - metabolism Low protein diet Male Males Malnutrition Mammals Medicine Metabolic syndrome Methylation Mitochondria Mitochondrial DNA Mothers Musculoskeletal system NADH NADH dehydrogenase Nicotinamide adenine dinucleotide Nutrition Offspring Oxidase Oxidases Oxidative phosphorylation Phosphorylation Physiology Pregnancy Promoter Regions, Genetic - drug effects Promoter Regions, Genetic - genetics Protein Binding - drug effects Proteins Pyrimidines Receptors, Glucocorticoid - metabolism RNA RNA, Messenger - genetics RNA, Messenger - metabolism Rodents Sex Sex Characteristics Swine Systematic review Transcription Transcription (Genetics) Transcription, Genetic - drug effects Veterinary Science |
| title | Maternal low-protein diet affects epigenetic regulation of hepatic mitochondrial DNA transcription in a sex-specific manner in newborn piglets associated with GR binding to its promoter |
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