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Filopodia-like protrusions of adjacent somatic cells shape the developmental potential of oocytes.

ABSTRACT: The oocyte must grow and mature before fertilization, thanks to a close dialogue with the somatic cells that surround it. Part of this communication is through filopodia-like protrusions, called transzonal projections (TZPs), sent by the somatic cells to the oocyte membrane. To investigate the contribution of TZPs to oocyte quality, we impaired their structure by generating a full knockout mouse of the TZP structural component myosin-X (MYO10). Using spinning disk and super-resolution microscopy combined with a machine-learning approach to phenotype oocyte morphology, we show that the lack of Myo10 decreases TZP density during oocyte growth. Reduction in TZPs does not prevent oocyte growth but impairs oocyte-matrix integrity. Importantly, we reveal by transcriptomic analysis that gene expression is altered in TZP-deprived oocytes and that oocyte maturation and subsequent early embryonic development are partially affected, effectively reducing mouse fertility. We propose that TZPs play a role in the structural integrity of the germline-somatic complex, which is essential for regulating gene expression in the oocyte and thus its developmental potential.

SUBMITTER: Crozet F

PROVIDER: S-EPMC10029974 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Filopodia-like protrusions of adjacent somatic cells shape the developmental potential of oocytes.

Crozet Flora F Letort Gaëlle G Bulteau Rose R Da Silva Christelle C Eichmuller Adrien A Tortorelli Anna Francesca AF Blévinal Joséphine J Belle Morgane M Dumont Julien J Piolot Tristan T Dauphin Aurélien A Coulpier Fanny F Chédotal Alain A Maître Jean-Léon JL Verlhac Marie-Hélène MH Clarke Hugh J HJ Terret Marie-Emilie ME

Life science alliance 20230321 6

The oocyte must grow and mature before fertilization, thanks to a close dialogue with the somatic cells that surround it. Part of this communication is through filopodia-like protrusions, called transzonal projections (TZPs), sent by the somatic cells to the oocyte membrane. To investigate the contribution of TZPs to oocyte quality, we impaired their structure by generating a full knockout mouse of the TZP structural component myosin-X (MYO10). Using spinning disk and super-resolution microscopy ...[more]

PMID: 36944420

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Project description:BackgroundOocyte maturation is crucial for female fertility and embryonic development, encompassing nuclear and cytoplasmic maturation. Supportive cells of follicles, such as granulosa cells, are essential for oocyte growth and maturation. Oocytes can achieve nuclear maturation without granulosa cells during in vitro maturation (IVM). However, there is still a higher chance of incomplete cytoplasmic maturation for these oocytes with mature nuclei compared with oocytes cultured with granulosa cells. Oocytes with incomplete cytoplasmic maturation have lower fertilization rates and developmental potential than mature ones, although underlying mechanisms are poorly understood. Identifying key genes and signaling pathways associated with oocyte cytoplasmic maturation can help further elucidate the maturing process of oocytes and understand the impact of immature oocytes on embryonic development, throwing insights into the strategy to improve the success rate of assisted reproductive technologies.ResultsOur study investigated murine oocytes maturing with and without granulosa cells. IVM without granulosa cells yielded oocytes with lower nuclear maturation rates than IVM with granulosa cells and in vivo maturation (IVO). Even though oocytes could achieve nuclear maturation without granulosa cells, they showed incomplete cytoplasmic maturation featuring higher levels of reactive oxygen species, lower mitochondrial density, and higher proportions of cells with abnormal distributions of cortical granules. Of note, oocytes with immature and mature cytoplasm had distinct transcriptional profiles. In the immature oocytes, we observed a deficient mRNA restoration of genes in crucial regulatory pathways of cellular growth and division, potentially affecting embryonic development. Differentially expressed genes (DEGs) between immature and mature oocytes were identified to be highly expressed in different pre-implantation stages, such as the MII oocyte, the 8-cell stage, and the ICM stage. Identified DEGs were enriched in key regulatory pathways of fertilization and embryonic development, such as energy and metabolic pathways. These observations indicated that the impeded development potential of oocytes with immature cytoplasm might be the result of abnormal gene expressions during oocyte maturation.ConclusionsWe show that granulosa cells are important for both nuclear and cytoplasmic maturation of oocytes. Abnormal gene expression in oocytes with incomplete cytoplasmic maturation may be associated with potential defects in fertilization and embryonic development.

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Filopodia-like protrusions of adjacent somatic cells shape the developmental potential of oocytes.

Publications

Filopodia-like protrusions of adjacent somatic cells shape the developmental potential of oocytes.

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