Overview of Gene Expression Dynamics during Human Oogenesis/Folliculogenesis

The oocyte transcriptome follows a tightly controlled dynamic that leads the oocyte to grow and mature. This succession of distinct transcriptional states determines embryonic development prior to embryonic genome activation. However, these oocyte maternal mRNA regulatory events have yet to be decod...

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Main Authors: Bastien Ducreux, Lucile Ferreux, Catherine Patrat, Patricia Fauque
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/25/1/33
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author Bastien Ducreux
Lucile Ferreux
Catherine Patrat
Patricia Fauque
author_facet Bastien Ducreux
Lucile Ferreux
Catherine Patrat
Patricia Fauque
author_sort Bastien Ducreux
collection DOAJ
description The oocyte transcriptome follows a tightly controlled dynamic that leads the oocyte to grow and mature. This succession of distinct transcriptional states determines embryonic development prior to embryonic genome activation. However, these oocyte maternal mRNA regulatory events have yet to be decoded in humans. We reanalyzed human single-oocyte RNA-seq datasets previously published in the literature to decrypt the transcriptomic reshuffles ensuring that the oocyte is fully competent. We applied trajectory analysis (pseudotime) and a meta-analysis and uncovered the fundamental transcriptomic requirements of the oocyte at any moment of oogenesis until reaching the metaphase II stage (MII). We identified a bunch of genes showing significant variation in expression from primordial-to-antral follicle oocyte development and characterized their temporal regulation and their biological relevance. We also revealed the selective regulation of specific transcripts during the germinal vesicle-to-MII transition. Transcripts associated with energy production and mitochondrial functions were extensively downregulated, while those associated with cytoplasmic translation, histone modification, meiotic processes, and RNA processes were conserved. From the genes identified in this study, some appeared as sensitive to environmental factors such as maternal age, polycystic ovary syndrome, cryoconservation, and in vitro maturation. In the future, the atlas of transcriptomic changes described in this study will enable more precise identification of the transcripts responsible for follicular growth and oocyte maturation failures.
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spelling doaj.art-fac97900e37f4ed297ca2adffa764c312024-01-10T14:57:54ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-12-012513310.3390/ijms25010033Overview of Gene Expression Dynamics during Human Oogenesis/FolliculogenesisBastien Ducreux0Lucile Ferreux1Catherine Patrat2Patricia Fauque3Université Bourgogne Franche-Comté-Equipe Génétique des Anomalies du Développement (GAD) INSERM UMR1231, 2 Rue Angélique Ducoudray, F-21000 Dijon, FranceFaculty of Medicine, Inserm 1016, Université de Paris Cité, F-75014 Paris, FranceFaculty of Medicine, Inserm 1016, Université de Paris Cité, F-75014 Paris, FranceUniversité Bourgogne Franche-Comté-Equipe Génétique des Anomalies du Développement (GAD) INSERM UMR1231, 2 Rue Angélique Ducoudray, F-21000 Dijon, FranceThe oocyte transcriptome follows a tightly controlled dynamic that leads the oocyte to grow and mature. This succession of distinct transcriptional states determines embryonic development prior to embryonic genome activation. However, these oocyte maternal mRNA regulatory events have yet to be decoded in humans. We reanalyzed human single-oocyte RNA-seq datasets previously published in the literature to decrypt the transcriptomic reshuffles ensuring that the oocyte is fully competent. We applied trajectory analysis (pseudotime) and a meta-analysis and uncovered the fundamental transcriptomic requirements of the oocyte at any moment of oogenesis until reaching the metaphase II stage (MII). We identified a bunch of genes showing significant variation in expression from primordial-to-antral follicle oocyte development and characterized their temporal regulation and their biological relevance. We also revealed the selective regulation of specific transcripts during the germinal vesicle-to-MII transition. Transcripts associated with energy production and mitochondrial functions were extensively downregulated, while those associated with cytoplasmic translation, histone modification, meiotic processes, and RNA processes were conserved. From the genes identified in this study, some appeared as sensitive to environmental factors such as maternal age, polycystic ovary syndrome, cryoconservation, and in vitro maturation. In the future, the atlas of transcriptomic changes described in this study will enable more precise identification of the transcripts responsible for follicular growth and oocyte maturation failures.https://www.mdpi.com/1422-0067/25/1/33folliculogenesismaturationoocyteRNA-seqtranscriptome
spellingShingle Bastien Ducreux
Lucile Ferreux
Catherine Patrat
Patricia Fauque
Overview of Gene Expression Dynamics during Human Oogenesis/Folliculogenesis
International Journal of Molecular Sciences
folliculogenesis
maturation
oocyte
RNA-seq
transcriptome
title Overview of Gene Expression Dynamics during Human Oogenesis/Folliculogenesis
title_full Overview of Gene Expression Dynamics during Human Oogenesis/Folliculogenesis
title_fullStr Overview of Gene Expression Dynamics during Human Oogenesis/Folliculogenesis
title_full_unstemmed Overview of Gene Expression Dynamics during Human Oogenesis/Folliculogenesis
title_short Overview of Gene Expression Dynamics during Human Oogenesis/Folliculogenesis
title_sort overview of gene expression dynamics during human oogenesis folliculogenesis
topic folliculogenesis
maturation
oocyte
RNA-seq
transcriptome
url https://www.mdpi.com/1422-0067/25/1/33
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