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Meiotic maturation failure in primary ovarian insufficiency: insights from a bovine model

  • Reproductive physiology and disease
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

Oocytes from women presenting primary ovarian insufficiency (POI) generate viable embryos at a lower rate than non-POI women, but the mechanisms responsible for the lower oocyte quality remain elusive. Due to the scarcity of human oocytes for research, animal models provide a promising way forward. We aimed at investigating the molecular events characterizing final maturation in POI oocytes in a well-defined POI-like bovine model.

Methods

Single-cell RNA-sequencing of bovine control and POI-like, GV, and MII oocytes (n = 5 per group) was performed. DEseq2 was used to identify differentially expressed genes. Further, a Gene set enrichment analysis and a transcriptomic meta-analysis between bovine and human oocytes were performed.

Results

In control cows, we found 2223 differentially expressed genes between the GV and MII stages. Specifically, the affected genes were related to RNA processing and transport, protein synthesis, organelle remodeling and reorganization, and metabolism. The meta-analysis with a set of young human oocytes at different maturation stages revealed 315 conserved genes through the GV-MII transition in cows and humans, mostly related to meiotic progression and cell cycle. Gene expression analysis between GV and MII of POI-like oocytes showed no differences in terms of differentially expressed genes, pointing towards a substantial failure to properly remodel the transcriptome in the POI model, and with the clustering analysis indicating that the cow’s genetic background had a higher impact than the oocyte’s maturation stage.

Conclusion

Overall, we have identified and characterized a valuable animal model of POI, paving the way to identifying new molecular mechanisms involved in POI.

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Funding

This project received intramural funding from the Eugin Group and funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 860960.

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Authors and Affiliations

  1. Basic Research Laboratory – Eugin Group, Barcelona, 08006, Spain

    Sara Pietroforte, Mina Popovic, Rita Vassena & Filippo Zambelli

  2. Department of Cell Biology, Physiology and Immunology, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, 08193, Spain

    Sara Pietroforte & Elena Ibáñez

  3. Reproductive and Developmental Biology Laboratory, Department of Veterinary Medicine and Animal Sciences, Università degli Studi di Milano, Lodi, 26900, Italy

    Pritha Dey, Alberto Maria Luciano, Valentina Lodde & Federica Franciosi

  4. Current address, Fecundis, Barcelona, 08006, Spain

    Rita Vassena

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  1. Sara Pietroforte
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Correspondence to Mina Popovic or Filippo Zambelli.

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Pietroforte, S., Dey, P., Ibáñez, E. et al. Meiotic maturation failure in primary ovarian insufficiency: insights from a bovine model. J Assist Reprod Genet (2024). https://doi.org/10.1007/s10815-024-03160-3

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