Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of follicular atresia in Chinese buffalo
•The follicles with different atresia status of buffalo were defined and their physiological status was detected.•PPARγ play important role in the lipid metabolism homeostasis of atresia follicle.•Bilirubin is involved in follicular atresia, and it may be the main force to prevent lipid peroxidation...
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| Veröffentlicht in: | The Journal of steroid biochemistry and molecular biology 2021-09, Vol.212, p.105944-105944, Article 105944 |
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| container_title | The Journal of steroid biochemistry and molecular biology |
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| creator | Cheng, Juanru Pan, Yu Yang, Sufang Wei, Yaochang Lv, Qiao Xing, Qinghua Zhang, Ruimen Sun, Le Qin, Guangsheng Shi, Deshun Deng, Yanfei |
| description | •The follicles with different atresia status of buffalo were defined and their physiological status was detected.•PPARγ play important role in the lipid metabolism homeostasis of atresia follicle.•Bilirubin is involved in follicular atresia, and it may be the main force to prevent lipid peroxidation in follicular cells.•Energy metabolism and nucleotide metabolism of atretic follicles were inhibited.
Follicular atresia is a complex physiological process, which results in the waste of follicles and oocytes from the ovary. Elucidating the physiological mechanism of follicular atresia will hopefully reverse the fate of follicles, thereby improve the reproductive efficiency of female animals. However, there are still many gaps to be filled during the follicular atresia process. In this study, we first comprehensively summarized and compared a variety of methods to classify Chinese buffalo follicles with different extent of atresia. Then follicular fluid and granulosa cells from the corresponding follicles with different extent of atresia were collected for non-targeted metabolomics and transcriptomics analysis, respectively. After the detection and analysis of 129 follicles, a reasonable classification standard was formed: on the basis of morphological classification, the relative concentrations of estradiol (E2) and progesterone (PROG) in the follicular fluid were determined, follicles with an estradiol-to-progesterone (E2/PROG) ratio >5 were classified as healthy follicles (HF), 1≤ E2/PROG ≤5 as early atretic follicles (EF) and E2/PROG |
| doi_str_mv | 10.1016/j.jsbmb.2021.105944 |
| format | Article |
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Follicular atresia is a complex physiological process, which results in the waste of follicles and oocytes from the ovary. Elucidating the physiological mechanism of follicular atresia will hopefully reverse the fate of follicles, thereby improve the reproductive efficiency of female animals. However, there are still many gaps to be filled during the follicular atresia process. In this study, we first comprehensively summarized and compared a variety of methods to classify Chinese buffalo follicles with different extent of atresia. Then follicular fluid and granulosa cells from the corresponding follicles with different extent of atresia were collected for non-targeted metabolomics and transcriptomics analysis, respectively. After the detection and analysis of 129 follicles, a reasonable classification standard was formed: on the basis of morphological classification, the relative concentrations of estradiol (E2) and progesterone (PROG) in the follicular fluid were determined, follicles with an estradiol-to-progesterone (E2/PROG) ratio >5 were classified as healthy follicles (HF), 1≤ E2/PROG ≤5 as early atretic follicles (EF) and E2/PROG <1 as late atretic follicles (LF). Correspondingly, follicles with granulosa cells apoptosis rate less than 15 % were divided into HF, 15%–25% were classified as EF and more than 25 % were classified as LF. The integration analysis of non-targeted metabolomics and transcriptomics highlights the following three aspects: (1) Atresia seriously damaged the lipid metabolism homeostasis of follicle, in which PPARγ play important roles. (2) Energy metabolism and nucleotide metabolism of atretic follicles were inhibited. (3) Bilirubin is involved in follicular atresia, and it may be the main force to prevent lipid peroxidation in follicular cells. In summary, results of this study provide new understanding of the molecular mechanisms of Chinese buffalo follicular atresia.</description><identifier>ISSN: 0960-0760</identifier><identifier>EISSN: 1879-1220</identifier><identifier>DOI: 10.1016/j.jsbmb.2021.105944</identifier><language>eng</language><publisher>Oxford: Elsevier Ltd</publisher><subject>17β-Estradiol ; Apoptosis ; Bilirubin ; Buffalo ; Energy metabolism ; Follicles ; Follicular atresia ; Follicular fluid ; Granulosa cells ; Homeostasis ; Integration ; LC–MS ; Lipid metabolism ; Lipid peroxidation ; Metabolism ; Metabolomics ; Molecular modelling ; Non-targeted metabolomics ; Oocytes ; Peroxisome proliferator-activated receptors ; Physiology ; Progesterone ; Transcriptomics</subject><ispartof>The Journal of steroid biochemistry and molecular biology, 2021-09, Vol.212, p.105944-105944, Article 105944</ispartof><rights>2021 Elsevier Ltd</rights><rights>Copyright Elsevier BV Sep 2021</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c364t-7abab345a659de92c65b81b8cce07a96405b5c48ad07424bc1cef39d5e1c79b03</citedby><cites>FETCH-LOGICAL-c364t-7abab345a659de92c65b81b8cce07a96405b5c48ad07424bc1cef39d5e1c79b03</cites><orcidid>0000-0001-7548-399X ; 0000-0002-7367-2233</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.jsbmb.2021.105944$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids></links><search><creatorcontrib>Cheng, Juanru</creatorcontrib><creatorcontrib>Pan, Yu</creatorcontrib><creatorcontrib>Yang, Sufang</creatorcontrib><creatorcontrib>Wei, Yaochang</creatorcontrib><creatorcontrib>Lv, Qiao</creatorcontrib><creatorcontrib>Xing, Qinghua</creatorcontrib><creatorcontrib>Zhang, Ruimen</creatorcontrib><creatorcontrib>Sun, Le</creatorcontrib><creatorcontrib>Qin, Guangsheng</creatorcontrib><creatorcontrib>Shi, Deshun</creatorcontrib><creatorcontrib>Deng, Yanfei</creatorcontrib><title>Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of follicular atresia in Chinese buffalo</title><title>The Journal of steroid biochemistry and molecular biology</title><description>•The follicles with different atresia status of buffalo were defined and their physiological status was detected.•PPARγ play important role in the lipid metabolism homeostasis of atresia follicle.•Bilirubin is involved in follicular atresia, and it may be the main force to prevent lipid peroxidation in follicular cells.•Energy metabolism and nucleotide metabolism of atretic follicles were inhibited.
Follicular atresia is a complex physiological process, which results in the waste of follicles and oocytes from the ovary. Elucidating the physiological mechanism of follicular atresia will hopefully reverse the fate of follicles, thereby improve the reproductive efficiency of female animals. However, there are still many gaps to be filled during the follicular atresia process. In this study, we first comprehensively summarized and compared a variety of methods to classify Chinese buffalo follicles with different extent of atresia. Then follicular fluid and granulosa cells from the corresponding follicles with different extent of atresia were collected for non-targeted metabolomics and transcriptomics analysis, respectively. After the detection and analysis of 129 follicles, a reasonable classification standard was formed: on the basis of morphological classification, the relative concentrations of estradiol (E2) and progesterone (PROG) in the follicular fluid were determined, follicles with an estradiol-to-progesterone (E2/PROG) ratio >5 were classified as healthy follicles (HF), 1≤ E2/PROG ≤5 as early atretic follicles (EF) and E2/PROG <1 as late atretic follicles (LF). Correspondingly, follicles with granulosa cells apoptosis rate less than 15 % were divided into HF, 15%–25% were classified as EF and more than 25 % were classified as LF. The integration analysis of non-targeted metabolomics and transcriptomics highlights the following three aspects: (1) Atresia seriously damaged the lipid metabolism homeostasis of follicle, in which PPARγ play important roles. (2) Energy metabolism and nucleotide metabolism of atretic follicles were inhibited. (3) Bilirubin is involved in follicular atresia, and it may be the main force to prevent lipid peroxidation in follicular cells. In summary, results of this study provide new understanding of the molecular mechanisms of Chinese buffalo follicular atresia.</description><subject>17β-Estradiol</subject><subject>Apoptosis</subject><subject>Bilirubin</subject><subject>Buffalo</subject><subject>Energy metabolism</subject><subject>Follicles</subject><subject>Follicular atresia</subject><subject>Follicular fluid</subject><subject>Granulosa cells</subject><subject>Homeostasis</subject><subject>Integration</subject><subject>LC–MS</subject><subject>Lipid metabolism</subject><subject>Lipid peroxidation</subject><subject>Metabolism</subject><subject>Metabolomics</subject><subject>Molecular modelling</subject><subject>Non-targeted metabolomics</subject><subject>Oocytes</subject><subject>Peroxisome proliferator-activated receptors</subject><subject>Physiology</subject><subject>Progesterone</subject><subject>Transcriptomics</subject><issn>0960-0760</issn><issn>1879-1220</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kUFv3CAQhVHVSN2m_QW9IPXSizdggzGHHqpV00SK1Et7RoDHu1gYtoAj5Q_0d4ete8ohpyfNfO9pRg-hT5TsKaH9zbyfs1nMviUtrRMuGXuDdnQQsqFtS96iHZE9aYjoyTv0PueZENJ1VOzQ3_tQ4Jh0cTHgOOGSdMg2uXOJi7MZ6zDiEENTdDpCgREvULSJftsmeATtMy4nwGsYIfknF46VsScdXF4uiVP03tnV64R1SZCdxi7gw8kFyIDNOk3axw_oqkqGj__1Gv2-_f7rcNc8_Pxxf_j20NiuZ6UR2mjTMa57LkeQre25GagZrAUitOwZ4YZbNuiRCNYyY6mFqZMjB2qFNKS7Rl-23HOKf1bIRS0uW_BeB4hrVi1nNb5lhFX08wt0jmsK9bpKCS67QYhLYLdRNsWcE0zqnNyi05OiRF26UbP61426dKO2bqrr6-aC-uujg6SydRAsjC6BLWqM7lX_M29qm6c</recordid><startdate>202109</startdate><enddate>202109</enddate><creator>Cheng, Juanru</creator><creator>Pan, Yu</creator><creator>Yang, Sufang</creator><creator>Wei, Yaochang</creator><creator>Lv, Qiao</creator><creator>Xing, Qinghua</creator><creator>Zhang, Ruimen</creator><creator>Sun, Le</creator><creator>Qin, Guangsheng</creator><creator>Shi, Deshun</creator><creator>Deng, Yanfei</creator><general>Elsevier Ltd</general><general>Elsevier BV</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7548-399X</orcidid><orcidid>https://orcid.org/0000-0002-7367-2233</orcidid></search><sort><creationdate>202109</creationdate><title>Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of follicular atresia in Chinese buffalo</title><author>Cheng, Juanru ; Pan, Yu ; Yang, Sufang ; Wei, Yaochang ; Lv, Qiao ; Xing, Qinghua ; Zhang, Ruimen ; Sun, Le ; Qin, Guangsheng ; Shi, Deshun ; Deng, Yanfei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c364t-7abab345a659de92c65b81b8cce07a96405b5c48ad07424bc1cef39d5e1c79b03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>17β-Estradiol</topic><topic>Apoptosis</topic><topic>Bilirubin</topic><topic>Buffalo</topic><topic>Energy metabolism</topic><topic>Follicles</topic><topic>Follicular atresia</topic><topic>Follicular fluid</topic><topic>Granulosa cells</topic><topic>Homeostasis</topic><topic>Integration</topic><topic>LC–MS</topic><topic>Lipid metabolism</topic><topic>Lipid peroxidation</topic><topic>Metabolism</topic><topic>Metabolomics</topic><topic>Molecular modelling</topic><topic>Non-targeted metabolomics</topic><topic>Oocytes</topic><topic>Peroxisome proliferator-activated receptors</topic><topic>Physiology</topic><topic>Progesterone</topic><topic>Transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cheng, Juanru</creatorcontrib><creatorcontrib>Pan, Yu</creatorcontrib><creatorcontrib>Yang, Sufang</creatorcontrib><creatorcontrib>Wei, Yaochang</creatorcontrib><creatorcontrib>Lv, Qiao</creatorcontrib><creatorcontrib>Xing, Qinghua</creatorcontrib><creatorcontrib>Zhang, Ruimen</creatorcontrib><creatorcontrib>Sun, Le</creatorcontrib><creatorcontrib>Qin, Guangsheng</creatorcontrib><creatorcontrib>Shi, Deshun</creatorcontrib><creatorcontrib>Deng, Yanfei</creatorcontrib><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Journal of steroid biochemistry and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cheng, Juanru</au><au>Pan, Yu</au><au>Yang, Sufang</au><au>Wei, Yaochang</au><au>Lv, Qiao</au><au>Xing, Qinghua</au><au>Zhang, Ruimen</au><au>Sun, Le</au><au>Qin, Guangsheng</au><au>Shi, Deshun</au><au>Deng, Yanfei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of follicular atresia in Chinese buffalo</atitle><jtitle>The Journal of steroid biochemistry and molecular biology</jtitle><date>2021-09</date><risdate>2021</risdate><volume>212</volume><spage>105944</spage><epage>105944</epage><pages>105944-105944</pages><artnum>105944</artnum><issn>0960-0760</issn><eissn>1879-1220</eissn><abstract>•The follicles with different atresia status of buffalo were defined and their physiological status was detected.•PPARγ play important role in the lipid metabolism homeostasis of atresia follicle.•Bilirubin is involved in follicular atresia, and it may be the main force to prevent lipid peroxidation in follicular cells.•Energy metabolism and nucleotide metabolism of atretic follicles were inhibited.
Follicular atresia is a complex physiological process, which results in the waste of follicles and oocytes from the ovary. Elucidating the physiological mechanism of follicular atresia will hopefully reverse the fate of follicles, thereby improve the reproductive efficiency of female animals. However, there are still many gaps to be filled during the follicular atresia process. In this study, we first comprehensively summarized and compared a variety of methods to classify Chinese buffalo follicles with different extent of atresia. Then follicular fluid and granulosa cells from the corresponding follicles with different extent of atresia were collected for non-targeted metabolomics and transcriptomics analysis, respectively. After the detection and analysis of 129 follicles, a reasonable classification standard was formed: on the basis of morphological classification, the relative concentrations of estradiol (E2) and progesterone (PROG) in the follicular fluid were determined, follicles with an estradiol-to-progesterone (E2/PROG) ratio >5 were classified as healthy follicles (HF), 1≤ E2/PROG ≤5 as early atretic follicles (EF) and E2/PROG <1 as late atretic follicles (LF). Correspondingly, follicles with granulosa cells apoptosis rate less than 15 % were divided into HF, 15%–25% were classified as EF and more than 25 % were classified as LF. The integration analysis of non-targeted metabolomics and transcriptomics highlights the following three aspects: (1) Atresia seriously damaged the lipid metabolism homeostasis of follicle, in which PPARγ play important roles. (2) Energy metabolism and nucleotide metabolism of atretic follicles were inhibited. (3) Bilirubin is involved in follicular atresia, and it may be the main force to prevent lipid peroxidation in follicular cells. In summary, results of this study provide new understanding of the molecular mechanisms of Chinese buffalo follicular atresia.</abstract><cop>Oxford</cop><pub>Elsevier Ltd</pub><doi>10.1016/j.jsbmb.2021.105944</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-7548-399X</orcidid><orcidid>https://orcid.org/0000-0002-7367-2233</orcidid></addata></record> |
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| subjects | 17β-Estradiol Apoptosis Bilirubin Buffalo Energy metabolism Follicles Follicular atresia Follicular fluid Granulosa cells Homeostasis Integration LC–MS Lipid metabolism Lipid peroxidation Metabolism Metabolomics Molecular modelling Non-targeted metabolomics Oocytes Peroxisome proliferator-activated receptors Physiology Progesterone Transcriptomics |
| title | Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of follicular atresia in Chinese buffalo |
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