Melatonin-induced demethylation of antioxidant genes increases antioxidant capacity through RORα in cumulus cells of prepubertal lambs
Physical damage and oxidative stress may occur in prepubertal cumulus cells, due to insufficient glutathione synthesis. To determine potential epigenetic mechanisms related to antioxidant effects of melatonin on ovine prepubertal cumulus cells, 30 lambs, 4-wk-old were randomly allocated into two gro...
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| Veröffentlicht in: | Free radical biology & medicine 2019-02, Vol.131, p.173-183 |
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| creator | Fang, Yi Zhang, Jinlong Li, Yihai Guo, Xiaofei Li, Junjie Zhong, Rongzhen Zhang, Xiaosheng |
| description | Physical damage and oxidative stress may occur in prepubertal cumulus cells, due to insufficient glutathione synthesis. To determine potential epigenetic mechanisms related to antioxidant effects of melatonin on ovine prepubertal cumulus cells, 30 lambs, 4-wk-old were randomly allocated into two groups: a control (C, n = 20) group and a melatonin (M, n = 10) group given a subcutaneous implant containing 18 mg melatonin. All lambs were superovulated (250 IU FSH and 250 IU eCG). Cumulus cells from germinal vesicle stage cumulus oocyte complexes (COCs) were collected by ovarian follicular aspiration and dissociated with hyaluronidase. Compared to the C group, the M group had greater superovulation, better antioxidant capacity, a higher proportion of fully expanded COCs and a lower proportion of apoptotic cumulus cells (P |
| doi_str_mv | 10.1016/j.freeradbiomed.2018.11.027 |
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The potential epigenetic mechanisms related to antioxidant effects of melatonin on ovine prepubertal cumulus cells. In addition to free radical scavenging by melatonin itself or mediating of its specific receptors MT1, melatonin also induced demethylation of antioxidant genes through nucleus binding site RORα to increase antioxidant capacity of cumulus cells. [Display omitted]
•Melatonin treatment of prepubertal lambs improves superovulation and antioxidant capacity of cumulus cells;•Melatonin improves cumulus cells expansion and survival in prepubertal lambs;•Increased antioxidant capacity is regulated by melatonin receptors MT1 and RORα;•Melatonin reduces methylation of SOD1, GPx4 and CAT regulated by nuclear binding site RORα.</description><identifier>ISSN: 0891-5849</identifier><identifier>EISSN: 1873-4596</identifier><identifier>DOI: 10.1016/j.freeradbiomed.2018.11.027</identifier><identifier>PMID: 30472366</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Absorbable Implants ; Animals ; Antioxidant ; Antioxidants - pharmacology ; C-Reactive Protein - genetics ; C-Reactive Protein - metabolism ; Catalase - genetics ; Catalase - metabolism ; Cell Proliferation - drug effects ; Cumulus cells ; Cumulus Cells - cytology ; Cumulus Cells - drug effects ; Cumulus Cells - metabolism ; Cyclooxygenase 2 - genetics ; Cyclooxygenase 2 - metabolism ; Epigenesis, Genetic ; Female ; Follicle Stimulating Hormone - pharmacology ; Glutathione - metabolism ; Hyaluronan Synthases - genetics ; Hyaluronan Synthases - metabolism ; Lamb ; Melatonin ; Melatonin - pharmacology ; Methylation ; Nuclear Receptor Subfamily 1, Group F, Member 1 - genetics ; Nuclear Receptor Subfamily 1, Group F, Member 1 - metabolism ; Phospholipid Hydroperoxide Glutathione Peroxidase - genetics ; Phospholipid Hydroperoxide Glutathione Peroxidase - metabolism ; Primary Cell Culture ; Proto-Oncogene Proteins c-bcl-2 - genetics ; Proto-Oncogene Proteins c-bcl-2 - metabolism ; Receptors, Melatonin - genetics ; Receptors, Melatonin - metabolism ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Serum Amyloid P-Component - genetics ; Serum Amyloid P-Component - metabolism ; Sexual Maturation - physiology ; Sheep ; Superovulation - drug effects ; Superoxide Dismutase-1 - genetics ; Superoxide Dismutase-1 - metabolism</subject><ispartof>Free radical biology & medicine, 2019-02, Vol.131, p.173-183</ispartof><rights>2018 Elsevier Inc.</rights><rights>Copyright © 2018 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c383t-1c944f880e64f4fcd1e9b0597cbf18d5b3a3207cbc6d36ffffd30c61308172063</citedby><cites>FETCH-LOGICAL-c383t-1c944f880e64f4fcd1e9b0597cbf18d5b3a3207cbc6d36ffffd30c61308172063</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.freeradbiomed.2018.11.027$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3549,27923,27924,45994</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30472366$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fang, Yi</creatorcontrib><creatorcontrib>Zhang, Jinlong</creatorcontrib><creatorcontrib>Li, Yihai</creatorcontrib><creatorcontrib>Guo, Xiaofei</creatorcontrib><creatorcontrib>Li, Junjie</creatorcontrib><creatorcontrib>Zhong, Rongzhen</creatorcontrib><creatorcontrib>Zhang, Xiaosheng</creatorcontrib><title>Melatonin-induced demethylation of antioxidant genes increases antioxidant capacity through RORα in cumulus cells of prepubertal lambs</title><title>Free radical biology & medicine</title><addtitle>Free Radic Biol Med</addtitle><description>Physical damage and oxidative stress may occur in prepubertal cumulus cells, due to insufficient glutathione synthesis. To determine potential epigenetic mechanisms related to antioxidant effects of melatonin on ovine prepubertal cumulus cells, 30 lambs, 4-wk-old were randomly allocated into two groups: a control (C, n = 20) group and a melatonin (M, n = 10) group given a subcutaneous implant containing 18 mg melatonin. All lambs were superovulated (250 IU FSH and 250 IU eCG). Cumulus cells from germinal vesicle stage cumulus oocyte complexes (COCs) were collected by ovarian follicular aspiration and dissociated with hyaluronidase. Compared to the C group, the M group had greater superovulation, better antioxidant capacity, a higher proportion of fully expanded COCs and a lower proportion of apoptotic cumulus cells (P < 0.05). Melatonin up-regulated mRNA expression of genes for melatonin receptors MT1 and nuclear binding site RORα, antioxidants (SOD1, GPx4 and CAT) and cumulus cell expansion (PTX3, HAS2 and PTGS2), as well as Bcl2, but down-regulated expression of Bax (P < 0.05). Regarding epigenetics, there were less methylation at five CpG sites of SOD1, three CpG sites of GPx4 and two CpG sites of CAT in M versus C groups (P < 0.05), leading to lower total methylation of SOD1, GPx4 and CAT promoters region on M group (P < 0.05). In a mechanistic study, addition of MT1 or RORα antagonist increased ROS and MDA concentrations, but decreased T-AOC, GPx, CAT and T-SOD concentrations (P < 0.05), whereas there were no significant difference between the melatonin and MT2 antagonist treatment groups for T-AOC, GPx, CAT and T-SOD concentrations. Furthermore, addition of RORα agonist decreased total DNA methylation of SOD1, GPx4 and CAT, with no significant difference after MT1 agonist treatment. These studies provided new information regarding epigenetic mechanisms by which melatonin promoted ovine prepubertal cumulus cells antioxidant through RORα, both in vitro and in vivo.
The potential epigenetic mechanisms related to antioxidant effects of melatonin on ovine prepubertal cumulus cells. In addition to free radical scavenging by melatonin itself or mediating of its specific receptors MT1, melatonin also induced demethylation of antioxidant genes through nucleus binding site RORα to increase antioxidant capacity of cumulus cells. [Display omitted]
•Melatonin treatment of prepubertal lambs improves superovulation and antioxidant capacity of cumulus cells;•Melatonin improves cumulus cells expansion and survival in prepubertal lambs;•Increased antioxidant capacity is regulated by melatonin receptors MT1 and RORα;•Melatonin reduces methylation of SOD1, GPx4 and CAT regulated by nuclear binding site RORα.</description><subject>Absorbable Implants</subject><subject>Animals</subject><subject>Antioxidant</subject><subject>Antioxidants - pharmacology</subject><subject>C-Reactive Protein - genetics</subject><subject>C-Reactive Protein - metabolism</subject><subject>Catalase - genetics</subject><subject>Catalase - metabolism</subject><subject>Cell Proliferation - drug effects</subject><subject>Cumulus cells</subject><subject>Cumulus Cells - cytology</subject><subject>Cumulus Cells - drug effects</subject><subject>Cumulus Cells - metabolism</subject><subject>Cyclooxygenase 2 - genetics</subject><subject>Cyclooxygenase 2 - metabolism</subject><subject>Epigenesis, Genetic</subject><subject>Female</subject><subject>Follicle Stimulating Hormone - pharmacology</subject><subject>Glutathione - metabolism</subject><subject>Hyaluronan Synthases - genetics</subject><subject>Hyaluronan Synthases - metabolism</subject><subject>Lamb</subject><subject>Melatonin</subject><subject>Melatonin - pharmacology</subject><subject>Methylation</subject><subject>Nuclear Receptor Subfamily 1, Group F, Member 1 - genetics</subject><subject>Nuclear Receptor Subfamily 1, Group F, Member 1 - metabolism</subject><subject>Phospholipid Hydroperoxide Glutathione Peroxidase - genetics</subject><subject>Phospholipid Hydroperoxide Glutathione Peroxidase - metabolism</subject><subject>Primary Cell Culture</subject><subject>Proto-Oncogene Proteins c-bcl-2 - genetics</subject><subject>Proto-Oncogene Proteins c-bcl-2 - metabolism</subject><subject>Receptors, Melatonin - genetics</subject><subject>Receptors, Melatonin - metabolism</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Serum Amyloid P-Component - genetics</subject><subject>Serum Amyloid P-Component - metabolism</subject><subject>Sexual Maturation - physiology</subject><subject>Sheep</subject><subject>Superovulation - drug effects</subject><subject>Superoxide Dismutase-1 - genetics</subject><subject>Superoxide Dismutase-1 - metabolism</subject><issn>0891-5849</issn><issn>1873-4596</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUFu1TAQhi0Eoo_CFZAlNmwS7NhxHLFCVaFIRZUqWFuOPe7zU2IHO0G8E3AeLsKZ6ui1EuzwZsYz_8x4_CH0hpKaEireHWqXAJK2g48T2LohVNaU1qTpnqAdlR2reNuLp2hHZE-rVvL-DL3I-UAI4S2Tz9EZI7xrmBA79OsLjHqJwYfKB7sasNjCBMv-WMI-Bhwd1qF4P70tFt9BgIx9MAl0Lt7fOaNnbfxyxMs-xfVuj29vbv_8LmJs1mkd14wNjGPeWs4J5nWAtOgRj3oa8kv0zOkxw6sHe46-fbz8enFVXd98-nzx4boyTLKloqbn3ElJQHDHnbEU-oG0fWcGR6VtB6ZZQ8rNCMuEK8cyYgRlRNKuIYKdo7envnOK31fIi5p83p6lA8Q1q4YySTjvelqk709Sk2LOCZyak590OipK1EZCHdQ_JNRGQlGqColS_fph0Dpsucfax68vgsuTAMq6PzwklY2HUAj4BGZRNvr_GnQPexWmYA</recordid><startdate>20190201</startdate><enddate>20190201</enddate><creator>Fang, Yi</creator><creator>Zhang, Jinlong</creator><creator>Li, Yihai</creator><creator>Guo, Xiaofei</creator><creator>Li, Junjie</creator><creator>Zhong, Rongzhen</creator><creator>Zhang, Xiaosheng</creator><general>Elsevier Inc</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>7X8</scope></search><sort><creationdate>20190201</creationdate><title>Melatonin-induced demethylation of antioxidant genes increases antioxidant capacity through RORα in cumulus cells of prepubertal lambs</title><author>Fang, Yi ; Zhang, Jinlong ; Li, Yihai ; Guo, Xiaofei ; Li, Junjie ; Zhong, Rongzhen ; Zhang, Xiaosheng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c383t-1c944f880e64f4fcd1e9b0597cbf18d5b3a3207cbc6d36ffffd30c61308172063</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Absorbable Implants</topic><topic>Animals</topic><topic>Antioxidant</topic><topic>Antioxidants - pharmacology</topic><topic>C-Reactive Protein - genetics</topic><topic>C-Reactive Protein - metabolism</topic><topic>Catalase - genetics</topic><topic>Catalase - metabolism</topic><topic>Cell Proliferation - drug effects</topic><topic>Cumulus cells</topic><topic>Cumulus Cells - cytology</topic><topic>Cumulus Cells - drug effects</topic><topic>Cumulus Cells - metabolism</topic><topic>Cyclooxygenase 2 - genetics</topic><topic>Cyclooxygenase 2 - metabolism</topic><topic>Epigenesis, Genetic</topic><topic>Female</topic><topic>Follicle Stimulating Hormone - pharmacology</topic><topic>Glutathione - metabolism</topic><topic>Hyaluronan Synthases - genetics</topic><topic>Hyaluronan Synthases - metabolism</topic><topic>Lamb</topic><topic>Melatonin</topic><topic>Melatonin - pharmacology</topic><topic>Methylation</topic><topic>Nuclear Receptor Subfamily 1, Group F, Member 1 - genetics</topic><topic>Nuclear Receptor Subfamily 1, Group F, Member 1 - metabolism</topic><topic>Phospholipid Hydroperoxide Glutathione Peroxidase - genetics</topic><topic>Phospholipid Hydroperoxide Glutathione Peroxidase - metabolism</topic><topic>Primary Cell Culture</topic><topic>Proto-Oncogene Proteins c-bcl-2 - genetics</topic><topic>Proto-Oncogene Proteins c-bcl-2 - metabolism</topic><topic>Receptors, Melatonin - genetics</topic><topic>Receptors, Melatonin - metabolism</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Serum Amyloid P-Component - genetics</topic><topic>Serum Amyloid P-Component - metabolism</topic><topic>Sexual Maturation - physiology</topic><topic>Sheep</topic><topic>Superovulation - drug effects</topic><topic>Superoxide Dismutase-1 - genetics</topic><topic>Superoxide Dismutase-1 - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fang, Yi</creatorcontrib><creatorcontrib>Zhang, Jinlong</creatorcontrib><creatorcontrib>Li, Yihai</creatorcontrib><creatorcontrib>Guo, Xiaofei</creatorcontrib><creatorcontrib>Li, Junjie</creatorcontrib><creatorcontrib>Zhong, Rongzhen</creatorcontrib><creatorcontrib>Zhang, Xiaosheng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Free radical biology & medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fang, Yi</au><au>Zhang, Jinlong</au><au>Li, Yihai</au><au>Guo, Xiaofei</au><au>Li, Junjie</au><au>Zhong, Rongzhen</au><au>Zhang, Xiaosheng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Melatonin-induced demethylation of antioxidant genes increases antioxidant capacity through RORα in cumulus cells of prepubertal lambs</atitle><jtitle>Free radical biology & medicine</jtitle><addtitle>Free Radic Biol Med</addtitle><date>2019-02-01</date><risdate>2019</risdate><volume>131</volume><spage>173</spage><epage>183</epage><pages>173-183</pages><issn>0891-5849</issn><eissn>1873-4596</eissn><abstract>Physical damage and oxidative stress may occur in prepubertal cumulus cells, due to insufficient glutathione synthesis. To determine potential epigenetic mechanisms related to antioxidant effects of melatonin on ovine prepubertal cumulus cells, 30 lambs, 4-wk-old were randomly allocated into two groups: a control (C, n = 20) group and a melatonin (M, n = 10) group given a subcutaneous implant containing 18 mg melatonin. All lambs were superovulated (250 IU FSH and 250 IU eCG). Cumulus cells from germinal vesicle stage cumulus oocyte complexes (COCs) were collected by ovarian follicular aspiration and dissociated with hyaluronidase. Compared to the C group, the M group had greater superovulation, better antioxidant capacity, a higher proportion of fully expanded COCs and a lower proportion of apoptotic cumulus cells (P < 0.05). Melatonin up-regulated mRNA expression of genes for melatonin receptors MT1 and nuclear binding site RORα, antioxidants (SOD1, GPx4 and CAT) and cumulus cell expansion (PTX3, HAS2 and PTGS2), as well as Bcl2, but down-regulated expression of Bax (P < 0.05). Regarding epigenetics, there were less methylation at five CpG sites of SOD1, three CpG sites of GPx4 and two CpG sites of CAT in M versus C groups (P < 0.05), leading to lower total methylation of SOD1, GPx4 and CAT promoters region on M group (P < 0.05). In a mechanistic study, addition of MT1 or RORα antagonist increased ROS and MDA concentrations, but decreased T-AOC, GPx, CAT and T-SOD concentrations (P < 0.05), whereas there were no significant difference between the melatonin and MT2 antagonist treatment groups for T-AOC, GPx, CAT and T-SOD concentrations. Furthermore, addition of RORα agonist decreased total DNA methylation of SOD1, GPx4 and CAT, with no significant difference after MT1 agonist treatment. These studies provided new information regarding epigenetic mechanisms by which melatonin promoted ovine prepubertal cumulus cells antioxidant through RORα, both in vitro and in vivo.
The potential epigenetic mechanisms related to antioxidant effects of melatonin on ovine prepubertal cumulus cells. In addition to free radical scavenging by melatonin itself or mediating of its specific receptors MT1, melatonin also induced demethylation of antioxidant genes through nucleus binding site RORα to increase antioxidant capacity of cumulus cells. [Display omitted]
•Melatonin treatment of prepubertal lambs improves superovulation and antioxidant capacity of cumulus cells;•Melatonin improves cumulus cells expansion and survival in prepubertal lambs;•Increased antioxidant capacity is regulated by melatonin receptors MT1 and RORα;•Melatonin reduces methylation of SOD1, GPx4 and CAT regulated by nuclear binding site RORα.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>30472366</pmid><doi>10.1016/j.freeradbiomed.2018.11.027</doi><tpages>11</tpages></addata></record> |
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| ispartof | Free radical biology & medicine, 2019-02, Vol.131, p.173-183 |
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| source | MEDLINE; ScienceDirect Journals (5 years ago - present) |
| subjects | Absorbable Implants Animals Antioxidant Antioxidants - pharmacology C-Reactive Protein - genetics C-Reactive Protein - metabolism Catalase - genetics Catalase - metabolism Cell Proliferation - drug effects Cumulus cells Cumulus Cells - cytology Cumulus Cells - drug effects Cumulus Cells - metabolism Cyclooxygenase 2 - genetics Cyclooxygenase 2 - metabolism Epigenesis, Genetic Female Follicle Stimulating Hormone - pharmacology Glutathione - metabolism Hyaluronan Synthases - genetics Hyaluronan Synthases - metabolism Lamb Melatonin Melatonin - pharmacology Methylation Nuclear Receptor Subfamily 1, Group F, Member 1 - genetics Nuclear Receptor Subfamily 1, Group F, Member 1 - metabolism Phospholipid Hydroperoxide Glutathione Peroxidase - genetics Phospholipid Hydroperoxide Glutathione Peroxidase - metabolism Primary Cell Culture Proto-Oncogene Proteins c-bcl-2 - genetics Proto-Oncogene Proteins c-bcl-2 - metabolism Receptors, Melatonin - genetics Receptors, Melatonin - metabolism RNA, Messenger - genetics RNA, Messenger - metabolism Serum Amyloid P-Component - genetics Serum Amyloid P-Component - metabolism Sexual Maturation - physiology Sheep Superovulation - drug effects Superoxide Dismutase-1 - genetics Superoxide Dismutase-1 - metabolism |
| title | Melatonin-induced demethylation of antioxidant genes increases antioxidant capacity through RORα in cumulus cells of prepubertal lambs |
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