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Single‐cell RNA‐Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation

The assembly of primordial follicles in mammals represents one of the most critical processes in ovarian biology. It directly affects the number of oocytes available to a female throughout her reproductive life. Premature depletion of primordial follicles contributes to the ovarian pathology primary...

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Autores principales: He, Yuanlin, Chen, Qiuzhen, Dai, Juncheng, Cui, Yiqiang, Zhang, Chi, Wen, Xidong, Li, Jiazhao, Xiao, Yue, Peng, Xiaoxu, Liu, Mingxi, Shen, Bin, Sha, Jiahao, Hu, Zhibin, Li, Jing, Shu, Wenjie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8282241/
https://www.ncbi.nlm.nih.gov/pubmed/34174788
http://dx.doi.org/10.1111/acel.13424
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author He, Yuanlin
Chen, Qiuzhen
Dai, Juncheng
Cui, Yiqiang
Zhang, Chi
Wen, Xidong
Li, Jiazhao
Xiao, Yue
Peng, Xiaoxu
Liu, Mingxi
Shen, Bin
Sha, Jiahao
Hu, Zhibin
Li, Jing
Shu, Wenjie
author_facet He, Yuanlin
Chen, Qiuzhen
Dai, Juncheng
Cui, Yiqiang
Zhang, Chi
Wen, Xidong
Li, Jiazhao
Xiao, Yue
Peng, Xiaoxu
Liu, Mingxi
Shen, Bin
Sha, Jiahao
Hu, Zhibin
Li, Jing
Shu, Wenjie
author_sort He, Yuanlin
collection PubMed
description The assembly of primordial follicles in mammals represents one of the most critical processes in ovarian biology. It directly affects the number of oocytes available to a female throughout her reproductive life. Premature depletion of primordial follicles contributes to the ovarian pathology primary ovarian insufficiency (POI). To delineate the developmental trajectory and regulatory mechanisms of oocytes during the process, we performed RNA‐seq on single germ cells from newborn (P0.5) ovaries. Three cell clusters were classified which corresponded to three cell states (germ cell cyst, cyst breakdown, and follicle) in the newborn ovary. By Monocle analysis, a uniform trajectory of oocyte development was built with a series of genes showed dynamic changes along the pseudo‐timeline. Gene Ontology term enrichment revealed a significant decrease in meiosis‐related genes and a dramatic increase in oocyte‐specific genes which marked the transition from a germ cell to a functional oocyte. We then established a network of regulons by using single‐cell regulatory network inference and clustering (SCENIC) algorithm and identified possible candidate transcription factors that may maintain transcription programs during follicle formation. Following functional studies further revealed the differential regulation of the identified regulon Id2 and its family member Id1, on the establishment of primordial follicle pool by using siRNA knockdown and genetic modified mouse models. In summary, our study systematically reconstructed molecular cascades in oocytes and identified a series of genes and molecular pathways in follicle formation and development.
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spelling pubmed-82822412021-07-16 Single‐cell RNA‐Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation He, Yuanlin Chen, Qiuzhen Dai, Juncheng Cui, Yiqiang Zhang, Chi Wen, Xidong Li, Jiazhao Xiao, Yue Peng, Xiaoxu Liu, Mingxi Shen, Bin Sha, Jiahao Hu, Zhibin Li, Jing Shu, Wenjie Aging Cell Original Articles The assembly of primordial follicles in mammals represents one of the most critical processes in ovarian biology. It directly affects the number of oocytes available to a female throughout her reproductive life. Premature depletion of primordial follicles contributes to the ovarian pathology primary ovarian insufficiency (POI). To delineate the developmental trajectory and regulatory mechanisms of oocytes during the process, we performed RNA‐seq on single germ cells from newborn (P0.5) ovaries. Three cell clusters were classified which corresponded to three cell states (germ cell cyst, cyst breakdown, and follicle) in the newborn ovary. By Monocle analysis, a uniform trajectory of oocyte development was built with a series of genes showed dynamic changes along the pseudo‐timeline. Gene Ontology term enrichment revealed a significant decrease in meiosis‐related genes and a dramatic increase in oocyte‐specific genes which marked the transition from a germ cell to a functional oocyte. We then established a network of regulons by using single‐cell regulatory network inference and clustering (SCENIC) algorithm and identified possible candidate transcription factors that may maintain transcription programs during follicle formation. Following functional studies further revealed the differential regulation of the identified regulon Id2 and its family member Id1, on the establishment of primordial follicle pool by using siRNA knockdown and genetic modified mouse models. In summary, our study systematically reconstructed molecular cascades in oocytes and identified a series of genes and molecular pathways in follicle formation and development. John Wiley and Sons Inc. 2021-06-26 2021-07 /pmc/articles/PMC8282241/ /pubmed/34174788 http://dx.doi.org/10.1111/acel.13424 Text en © 2021 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
He, Yuanlin
Chen, Qiuzhen
Dai, Juncheng
Cui, Yiqiang
Zhang, Chi
Wen, Xidong
Li, Jiazhao
Xiao, Yue
Peng, Xiaoxu
Liu, Mingxi
Shen, Bin
Sha, Jiahao
Hu, Zhibin
Li, Jing
Shu, Wenjie
Single‐cell RNA‐Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation
title Single‐cell RNA‐Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation
title_full Single‐cell RNA‐Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation
title_fullStr Single‐cell RNA‐Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation
title_full_unstemmed Single‐cell RNA‐Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation
title_short Single‐cell RNA‐Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation
title_sort single‐cell rna‐seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8282241/
https://www.ncbi.nlm.nih.gov/pubmed/34174788
http://dx.doi.org/10.1111/acel.13424
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