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In vivo and in vitro matured bovine oocytes present a distinct pattern of single-cell gene expression

Published online by Cambridge University Press:  20 October 2022

Lisandra C. Caetano Open the ORCID record for Lisandra C. Caetano [Opens in a new window] ,
Carolina G. Verruma Open the ORCID record for Carolina G. Verruma [Opens in a new window] ,
Fabio L.V. Pinaffi ,
Izabelle B. Jardim ,
Gilvan P. Furtado Open the ORCID record for Gilvan P. Furtado [Opens in a new window] ,
Luciano A. Silva ,
Cristiana L.M. Furtado Open the ORCID record for Cristiana L.M. Furtado [Opens in a new window]  and
Ana Carolina J. de Sá Rosa-e-Silva Open the ORCID record for Ana Carolina J. de Sá Rosa-e-Silva [Opens in a new window]
Lisandra C. Caetano
Affiliation:
Gynecology and Obstetrics Department, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, SP, Brazil
Carolina G. Verruma
Affiliation:
Genetics Department, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, SP, Brazil
Fabio L.V. Pinaffi
Affiliation:
Veterinary Medicine Department, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil Veterinary Clinical Sciences Department, College of Veterinary Medicine, Oklahoma State University, Stillwater, OK, USA
Izabelle B. Jardim
Affiliation:
Veterinary Medicine Department, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil
Gilvan P. Furtado
Affiliation:
Oswaldo Cruz Foundation, FIOCRUZ-Ceará, Sector of Biotechnology, Fortaleza, CE, Brazil
Luciano A. Silva
Affiliation:
Veterinary Medicine Department, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil
Cristiana L.M. Furtado*
Affiliation:
Gynecology and Obstetrics Department, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, SP, Brazil Drug Research and Development Center, Postgraduate Program in Translational Medicine, Federal University of Ceará, Fortaleza, CE, Brazil Experimental Biology Center, University of Fortaleza (UNIFOR), Fortaleza, CE, Brazil
Ana Carolina J. de Sá Rosa-e-Silva*
Affiliation:
Gynecology and Obstetrics Department, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, SP, Brazil
*
Authors for correspondence: Cristiana L. M. Furtado, Experimental Biology Center, Universisty of Fortaleza (UNIFOR), Fortaleza, CE, Brazil. E-mail: clibardim@gmail.com; Ana Carolina J. de Sá Rosa-e-Silva, Gynecology and Obstetrics Department, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, SP, Brazil. E-mail: anasars@fmrp.usp.br
Authors for correspondence: Cristiana L. M. Furtado, Experimental Biology Center, Universisty of Fortaleza (UNIFOR), Fortaleza, CE, Brazil. E-mail: clibardim@gmail.com; Ana Carolina J. de Sá Rosa-e-Silva, Gynecology and Obstetrics Department, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, SP, Brazil. E-mail: anasars@fmrp.usp.br
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Summary

Oocyte gene expression is a well controlled event that promotes gamete competence to undergo maturation, fertilization, and to support early embryo development, directly affecting reproductive outcomes. Considering that in vivo controlled ovarian stimulation or in vitro maturation (IVM) for the acquisition of mature oocytes has distinct implications for gene expression, we sought to evaluate the effects of these procedures on the expression of competence-related genes in single-cell oocytes. Healthy Nelore cows of reproductive age were synchronized to harvest in vivo matured oocytes; ovaries from slaughtered animals were used to obtain cumulus–oocyte complexes that were in vitro matured. Single-cell gene expression was performed using TaqMan Low-Density Arrays and 42 genes were evaluated. In silico analysis of protein interactions and Gene Ontology (GO) analysis was performed. Reduced gene expression was observed for 24 targets in IVM oocytes when compared with those of in vivo matured oocytes (P < 0.05). Differences ranged from 1.5-fold to 4.8-fold higher in in vivo oocytes and the BMP15 (5.28), GDF9 (6.23), NOBOX (7.25), HSPA8 (7.85) and MSX1 (11.00) showed the greatest fold increases. The strongest score of functional interactions was observed between the CDC20 and CKS2, with the differentially expressed gene CDC20 being the main marker behind GO enrichment. IVM negatively affected the expression of important genes related to oocyte competency, and showed higher expression levels in in vivo matured oocytes. In vivo controlled ovarian stimulation may be a better strategy to achieve proper oocyte competence and increase the success of assisted reproductive technologies.

Keywords

Assisted reproductive technologiesOocyte maturationReproductive outcomesSingle-cell gene expression
Type
Research Article
Information
Zygote , Volume 31 , Issue 1 , February 2023 , pp. 31 - 43
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Copyright
© The Author(s), 2022. Published by Cambridge University Press

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