Oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degeneration
Abstract Background In mammals, female fertility is influenced by the result of follicular development (ovulation or atresia). Follicular atresia is a complex physiological process that results in the degeneration of oocytes from the ovary. However, the molecular mechanisms of oocyte degeneration an...
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BMC
2025-02-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-025-11291-9 |
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| author | Yukun Song Erhan Hai Nan Zhang Yu Zhang Junlan Wang Xitong Han Jiaxin Zhang |
| author_facet | Yukun Song Erhan Hai Nan Zhang Yu Zhang Junlan Wang Xitong Han Jiaxin Zhang |
| author_sort | Yukun Song |
| collection | DOAJ |
| description | Abstract Background In mammals, female fertility is influenced by the result of follicular development (ovulation or atresia). Follicular atresia is a complex physiological process that results in the degeneration of oocytes from the ovary. However, the molecular mechanisms of oocyte degeneration and key protein markers of follicular atresia remain unclear. In this study, we investigated the complex transcriptional regulatory mechanisms and protein profiles in oocytes and follicular fluid in atretic follicle stages using single-cell RNA sequencing and tandem mass tag proteomics. Results First, through paired analysis of different follicle development stages, we identified 175 atresia-specific genes and eight candidate oocyte-secreted factors, including PKG1, YTHDF2, and MYC. Meanwhile, we also characterized unique features of the oocyte transcriptional landscape in the atretic follicle stage that displayed cell death-related transcriptional changes and mechanisms, such as autophagy (TBK1 and IRS4), necroptosis (PKR), and apoptosis (MARCKS). Moreover, we identified atresia-specific genes, namely FTH1, TF, and ACSL4, which may participate in regulation of oocyte ferroptosis in atretic follicles through a series of mechanisms including ferritinophagy, ferritin transport, and lipid metabolism. Additionally, we uncovered 333 differentially expressed proteins that may coordinate follicular atresia and revealed key pathways, such as negative regulation of angiogenesis, metabolic pathways, and transcription and mRNA splicing, that lead to oocyte degeneration. Finally, by combining transcriptome and proteomics analyses, we identified two oocyte-secreted biomarkers, PGK1 and ANGPT2, that may be associated with follicular atresia. Conclusions In conclusion, our work offers a thorough characterization of oocyte transcription mechanism and follicular fluid protein changes in ovine atretic follicles, which offers a crucial reference for analyzing the mechanism of follicular atresia and establishing an oocyte quality assessment system in sheep. |
| format | Article |
| id | doaj-art-8bd8e10781494fe4881e851df1185155 |
| institution | Kabale University |
| issn | 1471-2164 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj-art-8bd8e10781494fe4881e851df11851552025-02-02T12:10:14ZengBMCBMC Genomics1471-21642025-02-0126111910.1186/s12864-025-11291-9Oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degenerationYukun Song0Erhan Hai1Nan Zhang2Yu Zhang3Junlan Wang4Xitong Han5Jiaxin Zhang6Inner Mongolia Key Laboratory of Sheep & Goat Genetics Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural UniversityInner Mongolia Key Laboratory of Sheep & Goat Genetics Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural UniversityInner Mongolia Key Laboratory of Sheep & Goat Genetics Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural UniversityInner Mongolia Key Laboratory of Sheep & Goat Genetics Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural UniversityInner Mongolia Key Laboratory of Sheep & Goat Genetics Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural UniversityInner Mongolia Key Laboratory of Sheep & Goat Genetics Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural UniversityInner Mongolia Key Laboratory of Sheep & Goat Genetics Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural UniversityAbstract Background In mammals, female fertility is influenced by the result of follicular development (ovulation or atresia). Follicular atresia is a complex physiological process that results in the degeneration of oocytes from the ovary. However, the molecular mechanisms of oocyte degeneration and key protein markers of follicular atresia remain unclear. In this study, we investigated the complex transcriptional regulatory mechanisms and protein profiles in oocytes and follicular fluid in atretic follicle stages using single-cell RNA sequencing and tandem mass tag proteomics. Results First, through paired analysis of different follicle development stages, we identified 175 atresia-specific genes and eight candidate oocyte-secreted factors, including PKG1, YTHDF2, and MYC. Meanwhile, we also characterized unique features of the oocyte transcriptional landscape in the atretic follicle stage that displayed cell death-related transcriptional changes and mechanisms, such as autophagy (TBK1 and IRS4), necroptosis (PKR), and apoptosis (MARCKS). Moreover, we identified atresia-specific genes, namely FTH1, TF, and ACSL4, which may participate in regulation of oocyte ferroptosis in atretic follicles through a series of mechanisms including ferritinophagy, ferritin transport, and lipid metabolism. Additionally, we uncovered 333 differentially expressed proteins that may coordinate follicular atresia and revealed key pathways, such as negative regulation of angiogenesis, metabolic pathways, and transcription and mRNA splicing, that lead to oocyte degeneration. Finally, by combining transcriptome and proteomics analyses, we identified two oocyte-secreted biomarkers, PGK1 and ANGPT2, that may be associated with follicular atresia. Conclusions In conclusion, our work offers a thorough characterization of oocyte transcription mechanism and follicular fluid protein changes in ovine atretic follicles, which offers a crucial reference for analyzing the mechanism of follicular atresia and establishing an oocyte quality assessment system in sheep.https://doi.org/10.1186/s12864-025-11291-9Transcriptomics and proteomicsAtretic follicleOocyte degenerationFollicular fluidSheep |
| spellingShingle | Yukun Song Erhan Hai Nan Zhang Yu Zhang Junlan Wang Xitong Han Jiaxin Zhang Oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degeneration BMC Genomics Transcriptomics and proteomics Atretic follicle Oocyte degeneration Follicular fluid Sheep |
| title | Oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degeneration |
| title_full | Oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degeneration |
| title_fullStr | Oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degeneration |
| title_full_unstemmed | Oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degeneration |
| title_short | Oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degeneration |
| title_sort | oocyte transcriptomes and follicular fluid proteomics of ovine atretic follicles reveal the underlying mechanisms of oocyte degeneration |
| topic | Transcriptomics and proteomics Atretic follicle Oocyte degeneration Follicular fluid Sheep |
| url | https://doi.org/10.1186/s12864-025-11291-9 |
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