Enhancing Oocyte Quality in Aging Mice: Insights from Mesenchymal Stem Cell Therapy and FOXO3a Signaling Pathway Activation
Ovarian aging reduced the quality of oocytes, resulting in age-related female infertility. It is reported that mesenchymal stem cells (MSCs) therapy can improve age-related ovarian function decline and the success rate of in vitro maturation (IVM) in assisted reproductive therapy. In order to invest...
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| Veröffentlicht in: | Reproductive sciences (Thousand Oaks, Calif.) Calif.), 2024-08, Vol.31 (8), p.2392-2408 |
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| creator | Wang, Lingjuan Liu, Yang Song, Yinhua Mei, Qiaojuan Mou, Hongbei Wu, Jiachen Tang, Xinyu Ai, Jihui Li, Kezhen Xiao, Houxiu Han, Xiaotao Lv, Liqun Li, Huaibiao Zhang, Ling Xiang, Wenpei |
| description | Ovarian aging reduced the quality of oocytes, resulting in age-related female infertility. It is reported that mesenchymal stem cells (MSCs) therapy can improve age-related ovarian function decline and the success rate of
in vitro
maturation (IVM) in assisted reproductive therapy. In order to investigate the effectiveness and mechanisms of MSCs to enhance oocyte quality of cumulus oocyte complexes (COCs) in advanced age, this study focus on the respective functional improvement of oocytes and granulosa cells (GCs) from aging mice and further to explore and verify the possible mechanisms. Here, we studied a popular but significant protein of follicular development, Forkhead box O-3a (FOXO3a), which is a transcription factor that mediates a variety of cellular processes, but the functions of which in regulating oocyte quality in MSCs therapy still remain inconclusive. In this study, the RNA-seq data of metaphase II (MII) oocytes and GCs isolated from COCs confirmed that, GCs of immature follicles show the most potential to be the targeted cells of bone marrow mesenchymal stem cells (BMSCs) by FOXO3a signaling pathway. Furthermore, we demonstrated the effectiveness of BMSCs co-culture with aging COCs to enhance oocyte quality and found its mechanism to function via ameliorating the biological function of GCs by alleviating FOXO3a levels. These results provide significant fundamental research on MSCs therapy on ovarian aging, as well as offering guidance for raising the success rate of assisted reproductive technology such IVM in clinical and non-clinical settings.
Graphical Abstract |
| doi_str_mv | 10.1007/s43032-024-01509-8 |
| format | Article |
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in vitro
maturation (IVM) in assisted reproductive therapy. In order to investigate the effectiveness and mechanisms of MSCs to enhance oocyte quality of cumulus oocyte complexes (COCs) in advanced age, this study focus on the respective functional improvement of oocytes and granulosa cells (GCs) from aging mice and further to explore and verify the possible mechanisms. Here, we studied a popular but significant protein of follicular development, Forkhead box O-3a (FOXO3a), which is a transcription factor that mediates a variety of cellular processes, but the functions of which in regulating oocyte quality in MSCs therapy still remain inconclusive. In this study, the RNA-seq data of metaphase II (MII) oocytes and GCs isolated from COCs confirmed that, GCs of immature follicles show the most potential to be the targeted cells of bone marrow mesenchymal stem cells (BMSCs) by FOXO3a signaling pathway. Furthermore, we demonstrated the effectiveness of BMSCs co-culture with aging COCs to enhance oocyte quality and found its mechanism to function via ameliorating the biological function of GCs by alleviating FOXO3a levels. These results provide significant fundamental research on MSCs therapy on ovarian aging, as well as offering guidance for raising the success rate of assisted reproductive technology such IVM in clinical and non-clinical settings.
Graphical Abstract</description><identifier>ISSN: 1933-7191</identifier><identifier>ISSN: 1933-7205</identifier><identifier>EISSN: 1933-7205</identifier><identifier>DOI: 10.1007/s43032-024-01509-8</identifier><identifier>PMID: 38532230</identifier><language>eng</language><publisher>Cham: Springer International Publishing</publisher><subject>Aging - metabolism ; Aging - physiology ; Animals ; Coculture Techniques ; Embryology ; Female ; Forkhead Box Protein O3 - metabolism ; Granulosa Cells - metabolism ; Medicine ; Medicine & Public Health ; Mesenchymal Stem Cell Transplantation - methods ; Mesenchymal Stem Cells - metabolism ; Mice ; Obstetrics/Perinatology/Midwifery ; Oocytes - metabolism ; Regenerative Medicine: Original Article ; Reproductive Medicine ; Signal Transduction - physiology</subject><ispartof>Reproductive sciences (Thousand Oaks, Calif.), 2024-08, Vol.31 (8), p.2392-2408</ispartof><rights>The Author(s), under exclusive licence to Society for Reproductive Investigation 2024. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2024. The Author(s), under exclusive licence to Society for Reproductive Investigation.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c298t-507b805497a9ca2ad1566ee8f91fffa0f926096c3acbcc2c9f26cd2ce68883063</cites><orcidid>0000-0001-9510-116X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s43032-024-01509-8$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s43032-024-01509-8$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27923,27924,41487,42556,51318</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38532230$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Lingjuan</creatorcontrib><creatorcontrib>Liu, Yang</creatorcontrib><creatorcontrib>Song, Yinhua</creatorcontrib><creatorcontrib>Mei, Qiaojuan</creatorcontrib><creatorcontrib>Mou, Hongbei</creatorcontrib><creatorcontrib>Wu, Jiachen</creatorcontrib><creatorcontrib>Tang, Xinyu</creatorcontrib><creatorcontrib>Ai, Jihui</creatorcontrib><creatorcontrib>Li, Kezhen</creatorcontrib><creatorcontrib>Xiao, Houxiu</creatorcontrib><creatorcontrib>Han, Xiaotao</creatorcontrib><creatorcontrib>Lv, Liqun</creatorcontrib><creatorcontrib>Li, Huaibiao</creatorcontrib><creatorcontrib>Zhang, Ling</creatorcontrib><creatorcontrib>Xiang, Wenpei</creatorcontrib><title>Enhancing Oocyte Quality in Aging Mice: Insights from Mesenchymal Stem Cell Therapy and FOXO3a Signaling Pathway Activation</title><title>Reproductive sciences (Thousand Oaks, Calif.)</title><addtitle>Reprod. Sci</addtitle><addtitle>Reprod Sci</addtitle><description>Ovarian aging reduced the quality of oocytes, resulting in age-related female infertility. It is reported that mesenchymal stem cells (MSCs) therapy can improve age-related ovarian function decline and the success rate of
in vitro
maturation (IVM) in assisted reproductive therapy. In order to investigate the effectiveness and mechanisms of MSCs to enhance oocyte quality of cumulus oocyte complexes (COCs) in advanced age, this study focus on the respective functional improvement of oocytes and granulosa cells (GCs) from aging mice and further to explore and verify the possible mechanisms. Here, we studied a popular but significant protein of follicular development, Forkhead box O-3a (FOXO3a), which is a transcription factor that mediates a variety of cellular processes, but the functions of which in regulating oocyte quality in MSCs therapy still remain inconclusive. In this study, the RNA-seq data of metaphase II (MII) oocytes and GCs isolated from COCs confirmed that, GCs of immature follicles show the most potential to be the targeted cells of bone marrow mesenchymal stem cells (BMSCs) by FOXO3a signaling pathway. Furthermore, we demonstrated the effectiveness of BMSCs co-culture with aging COCs to enhance oocyte quality and found its mechanism to function via ameliorating the biological function of GCs by alleviating FOXO3a levels. These results provide significant fundamental research on MSCs therapy on ovarian aging, as well as offering guidance for raising the success rate of assisted reproductive technology such IVM in clinical and non-clinical settings.
Graphical Abstract</description><subject>Aging - metabolism</subject><subject>Aging - physiology</subject><subject>Animals</subject><subject>Coculture Techniques</subject><subject>Embryology</subject><subject>Female</subject><subject>Forkhead Box Protein O3 - metabolism</subject><subject>Granulosa Cells - metabolism</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Mesenchymal Stem Cell Transplantation - methods</subject><subject>Mesenchymal Stem Cells - metabolism</subject><subject>Mice</subject><subject>Obstetrics/Perinatology/Midwifery</subject><subject>Oocytes - metabolism</subject><subject>Regenerative Medicine: Original Article</subject><subject>Reproductive Medicine</subject><subject>Signal Transduction - physiology</subject><issn>1933-7191</issn><issn>1933-7205</issn><issn>1933-7205</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1v1DAQhi0EoqXwBzggH7kExnY-bG6rVUsrtVpQi8TNmvXaiavEWWynKOqfJ8u2HDnNaOadR6OHkPcMPjGA5nMqBQheAC8LYBWoQr4gp0wJUTQcqpfPPVPshLxJ6R6gKhWXr8mJkJXgXMApeTwPHQbjQ0s3o5mzpd8n7H2eqQ901R7mN97YL_QqJN92OVEXx4He2GSD6eYBe3qb7UDXtu_pXWcj7meKYUcvNj83Aumtb8PCWzDfMHe_caYrk_0DZj-Gt-SVwz7Zd0_1jPy4OL9bXxbXm69X69V1YbiSuaig2crD6w0qgxx3rKpra6VTzDmH4BSvQdVGoNkaw41yvDY7bmwtpRRQizPy8cjdx_HXZFPWg09meRiDHaekBYAoSwaNXKL8GDVxTClap_fRDxhnzUAfpOujdL1I13-l68PRhyf-tB3s7t_Js-UlII6BtKxCa6O-H6e4eEn_w_4BB_KNWA</recordid><startdate>20240801</startdate><enddate>20240801</enddate><creator>Wang, Lingjuan</creator><creator>Liu, Yang</creator><creator>Song, Yinhua</creator><creator>Mei, Qiaojuan</creator><creator>Mou, Hongbei</creator><creator>Wu, Jiachen</creator><creator>Tang, Xinyu</creator><creator>Ai, Jihui</creator><creator>Li, Kezhen</creator><creator>Xiao, Houxiu</creator><creator>Han, Xiaotao</creator><creator>Lv, Liqun</creator><creator>Li, Huaibiao</creator><creator>Zhang, Ling</creator><creator>Xiang, Wenpei</creator><general>Springer International Publishing</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><orcidid>https://orcid.org/0000-0001-9510-116X</orcidid></search><sort><creationdate>20240801</creationdate><title>Enhancing Oocyte Quality in Aging Mice: Insights from Mesenchymal Stem Cell Therapy and FOXO3a Signaling Pathway Activation</title><author>Wang, Lingjuan ; Liu, Yang ; Song, Yinhua ; Mei, Qiaojuan ; Mou, Hongbei ; Wu, Jiachen ; Tang, Xinyu ; Ai, Jihui ; Li, Kezhen ; Xiao, Houxiu ; Han, Xiaotao ; Lv, Liqun ; Li, Huaibiao ; Zhang, Ling ; Xiang, Wenpei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c298t-507b805497a9ca2ad1566ee8f91fffa0f926096c3acbcc2c9f26cd2ce68883063</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Aging - metabolism</topic><topic>Aging - physiology</topic><topic>Animals</topic><topic>Coculture Techniques</topic><topic>Embryology</topic><topic>Female</topic><topic>Forkhead Box Protein O3 - metabolism</topic><topic>Granulosa Cells - metabolism</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Mesenchymal Stem Cell Transplantation - methods</topic><topic>Mesenchymal Stem Cells - metabolism</topic><topic>Mice</topic><topic>Obstetrics/Perinatology/Midwifery</topic><topic>Oocytes - metabolism</topic><topic>Regenerative Medicine: Original Article</topic><topic>Reproductive Medicine</topic><topic>Signal Transduction - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Lingjuan</creatorcontrib><creatorcontrib>Liu, Yang</creatorcontrib><creatorcontrib>Song, Yinhua</creatorcontrib><creatorcontrib>Mei, Qiaojuan</creatorcontrib><creatorcontrib>Mou, Hongbei</creatorcontrib><creatorcontrib>Wu, Jiachen</creatorcontrib><creatorcontrib>Tang, Xinyu</creatorcontrib><creatorcontrib>Ai, Jihui</creatorcontrib><creatorcontrib>Li, Kezhen</creatorcontrib><creatorcontrib>Xiao, Houxiu</creatorcontrib><creatorcontrib>Han, Xiaotao</creatorcontrib><creatorcontrib>Lv, Liqun</creatorcontrib><creatorcontrib>Li, Huaibiao</creatorcontrib><creatorcontrib>Zhang, Ling</creatorcontrib><creatorcontrib>Xiang, Wenpei</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>Reproductive sciences (Thousand Oaks, Calif.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Lingjuan</au><au>Liu, Yang</au><au>Song, Yinhua</au><au>Mei, Qiaojuan</au><au>Mou, Hongbei</au><au>Wu, Jiachen</au><au>Tang, Xinyu</au><au>Ai, Jihui</au><au>Li, Kezhen</au><au>Xiao, Houxiu</au><au>Han, Xiaotao</au><au>Lv, Liqun</au><au>Li, Huaibiao</au><au>Zhang, Ling</au><au>Xiang, Wenpei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Enhancing Oocyte Quality in Aging Mice: Insights from Mesenchymal Stem Cell Therapy and FOXO3a Signaling Pathway Activation</atitle><jtitle>Reproductive sciences (Thousand Oaks, Calif.)</jtitle><stitle>Reprod. Sci</stitle><addtitle>Reprod Sci</addtitle><date>2024-08-01</date><risdate>2024</risdate><volume>31</volume><issue>8</issue><spage>2392</spage><epage>2408</epage><pages>2392-2408</pages><issn>1933-7191</issn><issn>1933-7205</issn><eissn>1933-7205</eissn><abstract>Ovarian aging reduced the quality of oocytes, resulting in age-related female infertility. It is reported that mesenchymal stem cells (MSCs) therapy can improve age-related ovarian function decline and the success rate of
in vitro
maturation (IVM) in assisted reproductive therapy. In order to investigate the effectiveness and mechanisms of MSCs to enhance oocyte quality of cumulus oocyte complexes (COCs) in advanced age, this study focus on the respective functional improvement of oocytes and granulosa cells (GCs) from aging mice and further to explore and verify the possible mechanisms. Here, we studied a popular but significant protein of follicular development, Forkhead box O-3a (FOXO3a), which is a transcription factor that mediates a variety of cellular processes, but the functions of which in regulating oocyte quality in MSCs therapy still remain inconclusive. In this study, the RNA-seq data of metaphase II (MII) oocytes and GCs isolated from COCs confirmed that, GCs of immature follicles show the most potential to be the targeted cells of bone marrow mesenchymal stem cells (BMSCs) by FOXO3a signaling pathway. Furthermore, we demonstrated the effectiveness of BMSCs co-culture with aging COCs to enhance oocyte quality and found its mechanism to function via ameliorating the biological function of GCs by alleviating FOXO3a levels. These results provide significant fundamental research on MSCs therapy on ovarian aging, as well as offering guidance for raising the success rate of assisted reproductive technology such IVM in clinical and non-clinical settings.
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| subjects | Aging - metabolism Aging - physiology Animals Coculture Techniques Embryology Female Forkhead Box Protein O3 - metabolism Granulosa Cells - metabolism Medicine Medicine & Public Health Mesenchymal Stem Cell Transplantation - methods Mesenchymal Stem Cells - metabolism Mice Obstetrics/Perinatology/Midwifery Oocytes - metabolism Regenerative Medicine: Original Article Reproductive Medicine Signal Transduction - physiology |
| title | Enhancing Oocyte Quality in Aging Mice: Insights from Mesenchymal Stem Cell Therapy and FOXO3a Signaling Pathway Activation |
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